Joanne Leslie is with the University of California, Los
Angeles, School of Public Health, Department of Community Health Sciences, and
The Pacific Institute for Womens Health, in Los Angeles, California, USA.
Elizabeth Ciemins is with the Los Angeles County Department of Health Services,
STD Program, in Los Angeles. Suzanne Bibi Essama is with the Tulane University
School of Public Health in New Orleans, Louisiana, USA.

Abstract

This article reviews and synthesizes existing nutritional
studies that provide gender-disaggregated data from sub-Saharan Africa. The
analytic focus is on female nutritional status across the life-span. However, it
was found that available data are biased towards preschool children and women of
reproductive age. As in other economically disadvantaged parts of the world, the
two most prevalent nutritional deficiencies among females in sub-Saharan Africa
are iron-deficiency anaemia and protein-energy malnutrition. In comparison with
other regions of the world, sub-Saharan African females seem to be nutritionally
better off than females in South Asia, but as malnourished as, or more
malnourished than, females elsewhere. Indirect indicators of nutritional status,
such as birthweight and maternal mortality, suggest that the nutritional
situation of women in Western Africa is poorer than that of women in Eastern and
Southern Africa. In comparison with males in sub-Saharan Africa, however, no
consistent pattern of female nutritional disadvantage was found.

Introduction

Increasingly, planners recognize that the health and nutrition
needs of females differ from those of males not only because of physiological
sex differences, but also because of gender differences. Culturally defined
roles and opportunities differ between males and females, leading to significant
differences in their knowledge of health and nutrition, their exposure to health
and nutrition risks, their access to care, and the social consequences they
experience as a result of poor health and nutrition. Therefore, a broad analysis
of the life circumstances of girls and women in Africa, not just a narrow focus
on biological aspects of nutritional status, is required in order to design
interventions that will be effective in improving the nutritional situation of
sub-Saharan African females [1, 2].

As in most developing countries, the nutritional status of
girls and women in sub-Saharan Africa is compromised by the cumulative and
synergistic effects of many risk factors. These factors include limited
availability of, or access to, food resources caused by natural and human-made
disasters; lack of control over inputs and resource allocation at the household
level; traditional feeding practices and other customs that limit womens
consumption of certain energy- or nutrient-rich foods; the energy demands of
heavy physical labour; the nutritional demands of frequent cycles of pregnancy
and lactation; and a high burden of infections with limited access to preventive
or curative care.

This overview of the nutritional implications of the multiple
time- and energy-demanding roles of sub-Saharan African women would lead the
reader to anticipate a high prevalence of malnutrition among sub-Saharan African
females. As this article makes clear, girls and women in this region are,
indeed, severely malnourished. However, given their limited economic resources
and their physically arduous lives, it is perhaps surprising that their
nutritional status is not even worse than it is.

Two caveats are worth noting at the outset. Available data on
nutrition in sub-Saharan Africa are biased towards pre-school children and women
of reproductive age. Thus, our analysis is limited by the scarcity of reliable
data on the female population outside these age groups. In addition, only rarely
are the available data nationally representative, or are there comparable data
over time.

Macronutrient disorders

Protein-energy malnutrition

As part of its Second Report on the World Nutrition Situation,
the United Nations Administrative Committee on Coordination/Subcommittee on
Nutrition (ACC/SCN) has published the most thorough and up-to-date global review
of the nutritional situation of women of reproductive age. Thus, the ACC/SCN
report provides the starting point for our assessment of the nutritional status
of females in sub-Saharan Africa. (The ACC/SCN database was compiled from about
340 small- and medium-scale studies of the nutritional status of women 15 to 49
years of age carried out since the late 1970s [3]).

The four anthropometric measures of nutritional status that
the ACC/SCN was able to use for their regional estimates of the prevalence of
protein-energy malnutrition among women were height, weight, body mass index
(BMI = weight in kilograms divided by height in meters squared), and arm
circumference. Adult women in sub-Saharan Africa were found to be surprisingly
tall. The average height is 158 cm, only 3 cm less than the average height of
161 cm for European women, whereas the mean height of women in South America and
most of Asia is only about 151 cm. Although these differences might be assumed
to be attributable to differences in genetic potential, the fact that the mean
height of women in China was found to be exactly the same as that of sub-Saharan
African women suggests that factors other than genetic potential must be
important determinants [3]. Short stature or stunting among adults is usually
taken as an indicator of cumulative malnutrition during childhood and
adolescence, and it is associated with a range of negative functional outcomes,
including reduced work capacity and poorer reproductive outcomes [4, 5]. The
cut-off point for the definition of stunting used by the ACC/SCN is 145 cm,
which is quite conservative. (As is discussed in our companion paper in this
issue [6], increased obstetrical risk has been associated with short stature
even at heights well above 145 cm). When this cut-off point was used, fewer than
5% of women in sub-Saharan Africa were classified as stunted, compared with more
than 15% in Middle America and Asia (excluding China), and about 12% in South
America.

The three other anthropometric measures of nutritional status
used in the ACC/SCN report are all more indicative of current nutritional
status. By these measures, women in sub-Saharan Africa also do fairly well in
comparison with women in other regions, but the differences are not so striking
as for height. Absolute weight, of course, is highly correlated with height.
Using 45 kg as the cut-off point (again quite conservatively), the ACC/SCN found
20% of African women to be underweight. This is about the same percentage as in
Middle America and China, more than in South America, but significantly less
than in Asia (excluding China), where 45% of women in South-East Asia and a
shocking 60% of women in South Asia are underweight, in large part because of
stunting. The percentage of women with arm circumferences below 22.5 cm could
only be calculated for sub-Saharan Africa, South Asia, and South-East Asia, and
these percentages followed very closely those for weight below 45 kg. The
relative position of women in sub-Saharan Africa is the worst when BMI, a
measure of relative thinness, is considered. When BMI below 18.5 is used as the
cut-off point, fewer than 20% of women in Middle America, South America, and
China, slightly more than 20% of women in sub-Saharan Africa, and about 40% of
women in South and South-East Asia are classified as excessively thin.

It is instructive to compare the regional information on child
nutritional status from the Second Report on the World Nutrition Situation with
the information on womens nutritional status (although, unfortunately, the
ACC/SCN does not report child nutritional status disaggregated by sex).
Anthropometric indicators of child nutrition have been more routinely collected
than information on adult nutritional status, so it is possible to estimate
regional trends in child nutrition over the past 20 years. It is when trends in
child nutrition are examined that the basis for the current concern about the
nutritional situation in sub-Saharan Africa becomes clearer. In all other
regions of the developing world, there was a marked decline between 1975 and
1990 in the prevalence of underweight pre-school children (defined as the
percentage of children below two standard deviations from the mean
weight-for-age in the age range zero to five years), ranging from a 50% decline
in South America to a 10% decline in South Asia. However, the prevalence of
child malnutrition in sub-Saharan Africa appears to have remained essentially
unchanged. Because of the continuing rapid rates of population growth in
sub-Saharan Africa, the absolute number of undernourished pre-school children
increased from 18.5 million in 1975 to 28.2 million in 1990. This means that the
present number of undernourished pre-school girls in sub-Saharan Africa is
almost as great as the total number of undernourished pre-school children in
1975. It also appears that the relative position of children in sub-Saharan
Africa is somewhat less favourable than the relative position of women when
compared with other regions of the developing world. Perhaps, because of their
smaller size and less mature immune systems, children have been less able than
adults to withstand the particularly harsh conditions that have been endured by
most sub-Saharan African countries over the last decade.

It would be speculative to try to assess the nutritional
situation of women and girls in individual countries, or to compare one part of
the region with another, because only aggregate regional estimates of
protein-energy malnutrition in sub-Saharan Africa are available from the Second
Report on the World Nutrition Situation. Although a substantial amount of
research has been carried out on the nutritional situation in sub-Saharan Africa
during the post-colonial period, the number, scope, and quality of the studies
vary substantially from one country to another, and many otherwise excellent
studies (particularly of child malnutrition) do not report sex-disaggregated
results. Two approaches have been taken in this paper to begin to disaggregate
the extent and diversity of the nutritional problems of females in sub-Saharan
Africa.

The first approach is to examine three indirect indicators
related to womens nutritional status that are available for essentially
all countries in the region. Table 1 presents the daily per capita energy
supply, the percentage of infants with low birthweight, and the maternal
mortality rate for all countries in sub-Saharan Africa for which such data could
be found. Table 1 and other tables are organized alphabetically by subregion,
and then alphabetically by country within each subregion. The four sub-regions -
Eastern, Middle, Southern, and Western Africa - and the countries within them
follow World Health Organization (WHO) usage [7]. For table 1, two World Bank
sources were consulted [8, 9], and where conflicting numbers were encountered,
both are presented in table 1. In most cases the numbers were close, but in a
few cases they were so different as to make one or both suspect.

Daily per capita energy supply is not specific to individual
households, much less to females within those households, but countries with a
daily per capita energy availability below 2,100 kcal are usually designated as
food insecure and believed to be at risk of having a substantial number of
food-deficient households [10]. We also know that in sub-Saharan Africa, women
who live in the most food-deficient households are usually the same women who do
the most physically demanding work and who give birth to and breastfeed the
largest number of infants. Therefore, without the ability to estimate a specific
number, it seems safe to assume that in any country with a daily per capita
energy supply below 2,100 kcal, there will be a reasonably high prevalence of
female malnutrition. Of the 37 countries in table 1 for which kilocalorie
estimates of daily per capita energy supply in 1989 were available, 12, or about
one-third, fell below 2,100 kcal.

Several studies in sub-Saharan Africa (as well as many studies
from other parts of the world) have demonstrated a relationship between
womens nutritional status - both current and past - and the birthweight of
their infants [11-13]. Although low birthweight can occur in the absence of
maternal malnutrition, and moderately malnourished women can give birth to
infants of adequate birthweight, the correlation between poor maternal
nutritional status and low birthweight at the aggregate level is sufficiently
strong that it is appropriate to use the percentage of low-birthweight infants
as an indirect indicator of female nutritional status. In general, we would
expect to find a substantial degree of malnutrition among women of reproductive
age (both stunting and thinness) in countries reporting a rate of more than 10%
low-birthweight infants. Twenty-five of the 37 countries in table 1 for which
information was available, or approximately two-thirds, reported more than 10%
low-birthweight infants in the mid-1980s.

Maternal mortality rate is also a reasonable indicator of
maternal nutritional status, particularly in the absence of adequate, accessible
prenatal and childbirth services. Maternal mortality is clearly a major problem
in the region; Africa has 20% of the worlds births but 40% of the
worlds maternal deaths [14]. Stunting is associated with a greater risk of
obstructed labour, and both obstructed labour and anaemia are among the major
causes of maternal mortality in sub-Saharan Africa [5]. Therefore, although the
maternal mortality rate does not differentiate among the different kinds of
nutritional problems that may affect girls and women, a high maternal mortality
rate is strongly suggestive of a high prevalence of female malnutrition.
Virtually all of the countries in table 1 had maternal mortality rates in 1980
of over 100 maternal deaths per 100,000 live births, and 13 of the 36 countries
for which data were available had maternal mortality rates above 500.

Comparisons among countries and even subregions of sub-Saharan
Africa based on the data in table 1 must be made quite cautiously because of
missing data and some lack of comparability among the data (e.g., maternal
mortality rates for some countries are based entirely on hospital data). In
addition, there are some inconsistencies in data between the two sources used to
compile this table. Nonetheless, with these caveats in mind, the data in table 1
do present some slightly surprising findings when the four subregions are
compared. In terms of food availability, table 1 suggests that Eastern Africa
and Middle Africa are the two most food-insecure parts of the region. In both
subregions, more than half the countries have a daily per capita energy supply
below 2,100 kcal, and for most of the remainder of the countries, per capita
energy availability is only slightly above the 2,100 kcal level. The food
availability situation appears to be distinctly better in Southern and Western
Africa.

Sources: World Bank: World Development Report 1992
[8] and Better Health in Africa [9].

a. Entries in kilocalories are from the 1992 World
Development Report. Those printed in bold are below 2,100 kilocalories per
person per day, which a recent FAD/WHO document labels as indicative of
household food insecurity based on a very low level of average food consumption
[10]. For countries with populations under one million, no data were available
from the World Development Report, and the estimated daily per capita energy
supply in 1985 as a percentage of requirement from Better Health in Africa [9]
is given. Although figures vary from country to country according to the age and
sex distribution of the population, the daily per capita energy supply needs to
be about 2,300 to be equivalent to 100% of average requirements.

b. Where two numbers are given, the first is from the
World Development Report [8] and the second from Better Health in Africa [9].
Where only one number is given, the two sources agreed, or only one source had
an entry for that indicator and country.

c. Before 1980.

d. Hospital data only.

e. Rural data only.

However, when the other two indicators related to female
nutritional status are examined, a somewhat different picture emerges. On the
basis of the percentage of low-birthweight infants and maternal mortality rates,
female malnutrition seems to be greatest in Western Africa (and, indeed, this is
consistent with the estimated subregional prevalences of anaemia, as shown in
table 3). In 10 of the 13 Western African countries for which there are data,
more than 10% of the infants have low birthweight; in the other 3 countries, the
percentage of low-birthweight babies is around 10%. Similarly, the number of
women dying per 100,000 live births is more than 500 in 6 of the 13 countries
for which there are data -and 100 to 500 in another 6 countries; the data for
one country, Mauritania, are difficult to interpret. In all 7 countries of
Middle Africa, the percentage of low-birthweight infants is greater than 10%,
similar to the situation in Western Africa. The figures for maternal mortality
are only slightly better in Middle than in Western Africa; 3 countries have more
than 500 maternal deaths per 100,000 live births and another 3 have from 100 to
500 deaths. In contrast, the situation in Eastern Africa looks noticeably
better. Among the 13 countries for which there are data, the percentage of
low-birthweight babies is greater than 10% in 7 countries, 10% in 3 countries,
and less than 10% in 2 countries; Zimbabwe is difficult to classify because the
rates given in the two sources, 15% and 6%, are so different. Only 2 countries
in Eastern Africa have more than 500 maternal deaths per 100,000 live births, 10
are in the 100 to 500 range, and 2 have rates below 100. The number of countries
in Southern Africa for which there are data is small, but both the percentage of
low-birthweight infants and maternal mortality rates seem to be similar to or
slightly better than those in Eastern Africa.

Unlike daily per capita energy availability, the percentage of
infants born with low birthweights and maternal mortality rates are specific to
females. Therefore, table 1 appears to suggest that Western and Middle Africa
are the two subregions where female malnutrition is the most prevalent, despite
overall better food security. A question that may warrant further investigation
is whether there are any dietary or behavioural factors in Eastern Africa that
contribute to protecting female nutritional status in the presence of extremely
low household food availability. Alternatively, it may be that access to health
care is better in Eastern and Southern Africa, thus to some extent compensating
for the negative effect of food insecurity.

Table 2 shows data that measure the nutritional status of
women more directly, using BMI as a measure of chronic energy deficiency. Table
2 also shows BMI data for men from the studies where they were available, but
discussion of the gender differences shown in table 2 is reserved for later in
this section. Although different cut-off points have been recommended, in
general a BMI below 18 or 18.5 is considered excessively thin, and such a person
is categorized as suffering from chronic energy deficiency. It should be noted
that although 18.5 seems to be an appropriate cut-off in terms of obstetrical
risk, a lower cut-off, perhaps as low as 16, is more predictive of increased
morbidity risk [1].

Among the countries from Eastern Africa with BMI data
available, it is clear that the situation is most severe in Ethiopia, with half
the women suffering from chronic energy deficiency. Twelve percent of women in
the Zimbabwe study, and probably a similar percentage in the Kenya study, would
be considered malnourished. For Middle Africa, data are only available from two
studies done in Zaire. Although the data are not presented in terms of
percentages below a cut-off, the relatively low range of the mean BMI values
(19.7 to 21.7) suggests that the percentage of women suffering from chronic
energy deficiency in these Zairian populations would be lower than in Ethiopia,
but higher than in Zimbabwe or Kenya. As far as Western Africa is concerned,
except for Côte dIvoire, where the mean BMI of women is similar to
that found in the Kenya study, the BMI data support the conclusion of
substantial female malnutrition suggested by the indirect indicators in table 1.
The data in table 2 are consistent with the estimated regional average of 21% of
women in sub-Saharan Africa who have a BMI below 18.5 [3].

It seems reasonably clear from the information presented in
tables 1, 2, and 4 (discussed in more detail in the next section) that the
problem of protein-energy deficiency is of considerable magnitude among females
in sub-Saharan Africa, with somewhere in the range of 5% to 10% of girls
suffering from acute protein-energy malnutrition, and 20% to 40% suffering from
chronic protein-energy malnutrition. Among adult women, from 1% to 6% may suffer
from severe chronic energy deficiency (chronic energy deficiency based on low
BMI), and from 10% to 40% may suffer from mild to moderate chronic energy
deficiency. In acute famine situations, of course, the proportion of females
suffering from acute protein-energy malnutrition will be much higher.

Obesity

Although inadequate energy intake is certainly the major
macronutritional problem among females in sub-Saharan Africa, it is important to
assess the prevalence of excess energy intake or obesity as well. Obesity is
known to substantially increase the risk of many chronic diseases, and with the
decline in the rates of many infectious diseases and increasing life expectancy,
a rapid increase in the prevalence of non-communicable diseases can be expected
in the near future in sub-Saharan Africa [24]. The prevalence of obesity is a
question that has received little attention from researchers concerned with
nutrition in sub-Saharan Africa, so relevant data are extremely limited. One of
the few studies to examine simultaneously the prevalence of chronic energy
deficiency and obesity in the same population groups was a comparative study of
adult nutritional status in India, Ethiopia, and Zimbabwe [16]. In the Ethiopian
population, there was a high prevalence of chronic energy deficiency (BMI was
less than 18.5 in 58% of women and less than 16 in 6%) and essentially no
obesity, defined as BMI greater than 25. In contrast, in the Zimbabwean
population, 12% of women had a BMI below 18.5 (of whom only 1% were below 16)
and 17% were defined as obese, with 2.5% having a BMI over 30. It is clear that
a high prevalence of chronic energy deficiency is correlated with a low
prevalence of obesity and vice versa, but also that moderate prevalences of both
can be found in the same population.

In Zimbabwe, the average BMI for females was reported to be 22
(standard deviation, 2.3). This figure is not dissimilar to the average BMI
reported for females in a number of other sub-Saharan African populations (see
table 2). Therefore, it seems probable that in at least some countries in the
region, we could expect to find a prevalence of obesity among adult women in the
range of 5% to 10%.

Micronutrient
deficiencies

Iron-deficiency, anaemia

Iron-deficiency anaemia is the most common nutritional
deficiency in the world, and given that it particularly affects pre-school
children and women of reproductive age, it is undoubtedly the most wide spread
nutritional problem affecting girls and women in sub-Saharan Africa. It is
generally accepted that about half the anaemia worldwide is due to iron
deficiency, and there is emerging evidence that low iron stores, even in the
absence of anaemia, can have negative functional consequences [3,7]. Therefore,
the prevalence of iron-deficiency anaemia can be taken as a minimum estimate of
the problems of both anaemia and iron deficiency.

Other important causes of anaemia, in addition to diets that
are deficient in iron, folate, or vitamin B12, are haemolysis due to malaria and
haemorrhage due to hookworm or schistosomiasis. In many African countries,
genetic diseases, such as sickle-cell anaemia, and human immunodeficiency virus
(HIV) infection can also lead to severe anaemia.

A publication prepared jointly by the Maternal Health and Safe
Motherhood Programme and the Nutrition Programme of WHO gives the most recent
estimates of the prevalence of nutritional anaemias in women in the world based
on studies carried out since 1970 [7]. Table 3 presents data for the four
sub-Saharan African subregions on the number and percentage of women with
haemoglobin levels below normal, most of which is attributable to iron
deficiency. The cut-offs used by WHO were less than 120 g/L haemoglobin for
non-pregnant adult women and less than 110 g/L for pregnant women; almost all
studies in the review by WHO included only women of reproductive age.

The relative nutritional situation of women by subregion in
terms of nutritional anaemia is quite similar to the situation presented in
table 1. Table 3 suggests that although women in Western Africa have the highest
prevalence of nutritional anaemia, the prevalences in Western Africa, Middle
Africa, and Eastern Africa are quite similar, while women in Southern Africa are
definitely less anaemic. The better situation of women in Southern Africa has
been attributed by some to the widespread use of iron cooking pots in this
region [7].

One disturbing finding of the Second Report on the World
Nutrition Situation is the apparent increase in iron deficiency in sub-Saharan
Africa and many other regions of the developing world except for the Near East,
North Africa, and South America. Although the ACC/SCN cautions that estimates of
the trends over time in the prevalence of anaemia should be considered quite
tentative, their data suggest that the prevalence of anaemia among non-pregnant
adult women of reproductive age in sub-Saharan Africa was around 37% from the
mid-1970s to the mid-1980s, and had increased to about 46% by the late 1980s.
Given the population increase over this time, an unavoidable conclusion is that
the absolute number of anaemic women in sub-Saharan Africa has probably
increased quite dramatically in the past decade. Part of the reason for the
increase in iron-deficiency anaemia is that the iron density in the diet appears
to be decreasing rather than increasing in sub-Saharan Africa and in most other
parts of the developing world. Although dietary iron density in sub-Saharan
Africa appears relatively good compared with other parts of the developing world
(7 to 8 mg per 1,000 kcal), the percentage of dietary iron from animal sources
is lower than for any region except South Asia, and the general bioavailability
of the dietary iron must be quite low.

Anaemia during pregnancy is widely recognized as one of the
major health and nutritional problems among pregnant women in sub-Saharan Africa
[5]. Factors that contribute to the high incidence of anaemia among pregnant
women in the region include poor dietary practices during pregnancy due to
sociocultural food taboos, infection, malabsorption, malaria, and increased
foetal demand. A case-control study of 122 pregnant anaemic women in Nigeria
[25] found that women were aware that they were at high risk for anaemia, but
their traditional preventive practices against anaemia proved
ineffective.

Iodine-deficiency disorders

Iodine-deficiency disorders exist in most regions of the
world, although usually in pockets, rather than throughout a country.
Iodine-deficient environments are those in which iodine, which is normally
supplied from soil and water, has been leached from the topsoil by rain,
flooding, glaciation, or snow. These environments tend to be either mountainous
inland regions or floodplains. Iodine deficiency is less strongly correlated
with food insecurity than are protein-energy malnutrition and iron-deficiency
anaemia. It is rare to encounter iodine deficiencies in populations living near
the sea or where the soil has adequate iodine, regardless of how impoverished or
subject to seasonal food shortages they may be.

The main manifestations of iodine deficiency are goitre,
impaired mental function, and increased rates of foetal wastage, stillbirths,
and infant deaths. Severe mental and neurological impairment, known as
cretinism, occurs among infants born to mothers who are seriously iodine
deficient.

The extent of iodine-deficiency disorders is usually assessed
by the prevalence of goitre in affected populations, although this understates
the number of people affected by iodine-deficiency disorders, particularly if
those suffering from reversible lethargy or mild mental impairment associated
with iodine deficiency are included. The ACC/SCN estimates that the prevalence
of goitre in Africa is about 8%. In Africa there are 39 million people with
goitre, half a million with overt cretinism, and another 227 million who are
estimated to be at risk for iodine-deficiency disorders [3, 26]. The ratio of
those at risk for iodine-deficiency disorders to those with goitre is extremely
high in Africa, reflecting, in part, the lack of control programmes, and
suggesting that iodine-deficiency disorders will continue to be a serious public
health problem in this region for many years to come.

Iodine-deficiency disorders are of particular concern among
women for two reasons. First, the range of functional consequences of iodine
deficiency is broader for women than for men, since it includes severe negative
reproductive outcomes for both mothers and infants [26]. In addition to the
broader range of functional consequences, the prevalence of goitre appears to be
significantly higher among females than among males in virtually all studies
with sex-disaggregated data [27]. In one Africa-specific study that reported
sex-disaggregated data from Zaire, Thilly et al. [28] found a significantly
higher prevalence of goitre among females than males at all ages from 10 years
upwards. The prevalence of visible and voluminous goitres in the age range of
peak prevalence (20 to 30 years) was almost 50% among females and about 20%
among males.

Vitamin A deficiency

Vitamin A deficiency, as defined by eye damage (ranging from
reversible night blindness through ulceration of the cornea to permanent
scarring and blindness), has been identified as a widespread public health
problem in at least 37 countries [3]. Each year it is estimated that between
250,000 and 500,000 pre-school-age children go blind from vitamin A deficiency,
and that within months of going blind, two-thirds of these children die [3]. In
addition, there is growing evidence that even children who do not necessarily
have eye signs may have subclinical vitamin A deficiency that puts them at
greater risk for morbidity and mortality from infectious diseases. Although all
children older than six months, as well as pregnant and lactating women, are at
risk for vitamin A deficiency, the peak prevalence seems to fall in the age
range of two to four years [29]. The literature supports the general finding of
a higher prevalence of eye damage due to vitamin A deficiency among
pre-school-age boys than girls [30]. It is not well established whether adult
men are similarly at greater risk compared with adult women, because few studies
have been done on vitamin A deficiency among adults. However, in a small number
of somewhat older country-specific studies from South Africa, Ethiopia, and
Rwanda, higher deficiency rates were found among adult men than adult women
[31-33].

In Africa about 7.2% of pre-school-age children (1.3 million)
are estimated to have eye damage due to vitamin A deficiency, and another 7.2
million suffer from a mild to moderate deficiency [3, 30]. The proportion of the
pre-school-age population affected in Africa is similar to the proportion in
most other parts of the developing world. Within the sub-Saharan African region,
the areas most affected are Eastern Africa, Southern Africa, and the Sahelian
parts of Western Africa. Populations living where red palm oil is produced or
distributed, that is, along the coastal parts of Western Africa and in some
parts of Central Africa, are reasonably well protected against vitamin A
deficiency.

Gender differences in malnutrition in
sub-Saharan Africa

Throughout the world, differences between males and females in
the prevalence of micronutrient deficiencies appear to be substantially
attributable to biological differences between the sexes. The higher prevalence
of iron-deficiency anaemia found among adolescent girls and adult women, for
example, is due primarily to the increased iron losses associated with
menstruation and the increased iron demands of pregnancy and lactation, although
this biological risk can be exacerbated by female diets that are lower in animal
protein or, in some cases, a higher prevalence of hookworm or malaria among
females [34]. Similarly, higher prevalences of iodine-deficiency disorders among
adult women and of vitamin A deficiency among pre-school-age boys (and perhaps
among older males) are documented by studies carried out in many different
cultural settings and appear to be primarily physiological, although the
specific mechanisms are less well understood than in the case of iron-deficiency
anaemia. In addition, there may be local dietary practices that enhance or
reduce the biological gender differences.

In contrast, as far as macronutrient disorders are concerned,
there are no underlying physiological reasons to expect differences between
males and females in the prevalence of thinness or obesity. Where such a pattern
does emerge, behavioural and cultural factors must provide the explanation.
Although there are significant differences in the roles and opportunities of
males and females in sub-Saharan Africa, no widespread pattern of gender
differences in protein-energy malnutrition has emerged from studies to date [35,
36]. On the basis of recent sex-disaggregated Demographic and Health Survey data
for children (see table 4), BMI data for adult men and women (see table 2), a
secondary analysis of somewhat older height and weight data from Eveleth and
Tanners Worldwide Variation in Human Growth [37] undertaken by Svedberg
[36], and other country-specific studies [see, for example, refs. 22, 38, and
39], it seems clear that in contrast to the situation in South Asia, in
sub-Saharan Africa there is no significant pattern of female disadvantage
according to anthropometric measures of nutritional status.

In his extensive analysis of gender bias in undernutrition in
sub-Saharan Africa, Svedberg actually proposed that the slight anthropometric
advantage shown by girls, women, or both in many countries may suggest a
historical pattern of preferential treatment of females due to the high value
placed on womens agricultural labour [36]. On the basis of a study of
gender biases among the Mukogodo of Kenya, Cronk [40] suggested that favouritism
towards daughters occurred as a result of lowered socio-economic status. In a
case study in south-central Ethiopia, Vesti [15] found that females scored
significantly better than males on weight-for age measurements, but only within
the lowest income bracket. However, given that there are also a number of
studies in sub-Saharan Africa that report dietary discrimination against females
[see, for example, refs. 41-43], any firm conclusion of a nutritionally
advantaged position of females in the region seems premature.

One particularly interesting report of gender differences in
dietary intake comes from a study of child-feeding practices in Zinder, Niger.
Field research conducted by CARE on traditional knowledge and practices related
to child care and feeding revealed that in some villages girls were weaned one
month later than boys. It was traditionally believed that an excess of
breastmilk would make a child stupid, and accordingly boys were weaned earlier
so that they would be intelligent and have a better chance of
success in school [44]. Although this practice may be beneficial to girls
nutrition in the short run, it is actually motivated by a lower value placed on
education for females, which may be detrimental to female health and nutritional
status in the longer run. A similar gender difference in breastfeeding patterns
was reported in a study of women in Dakar, Senegal, and the surrounding area,
where girls were breastfed up to 24 months and boys only to 18 months. However,
no link with intelligence was made [45]. It is quite likely that the aggregate
finding of little gender difference in anthropometric measures of protein-energy
malnutrition in sub-Saharan Africa reflects the cumulative effect of a number of
specific behaviours and practices, some of which may favour females and some of
which may favour males. In specific settings or during certain seasons,
significant gender differences have been reported. (See appendix 1 for further
examples).

a. Data were kindly provided by Hill of the
World sank They are assembled from Demographic and Health survey Reports and are
for all sub-Saharan African countries for which data on these indicators were
available.

b. Child mortality is usually considered most
indicative of child nutritional status.

c. For children 3-36 months old, percentage below 2
SD.

d. Percentage of children under age five with diarrhoea
during the two weeks preceding the survey.

Conclusion

As in other parts of the developing world, the two most
prevalent nutritional deficiencies among females in sub-Saharan Africa are
iron-deficiency anaemia and protein-energy malnutrition. Evidence for other
micronutrient deficiencies among girls and women in the region is quite limited,
but undoubtedly iodine-deficiency disorders are a major problem in many inland
parts of sub-Saharan Africa, and vitamin A deficiency is probably quite
prevalent in rural Sahelian communities where there are significant seasonal
fluctuations in quantity and quality of the diet.

In comparison with other regions of the world, sub-Saharan
African females seem to be nutritionally better off than females in South Asia,
but as malnourished as, or more malnourished than, females in most other parts
of the developing world. The nutritional situation of females in Western Africa
seems to be poorer than in other parts of the region. In contrast with South
Asia, there is no consistent pattern of a higher prevalence of protein-energy
malnutrition among females than males, despite a generally higher work burden
among adult women than among men in sub-Saharan Africa. However, small-scale
studies from a few countries have found evidence of discrimination against or
disadvantage experienced by females in breastfeeding and dietary patterns, and
the lack of attention to gender differences in much of the work that has been
done on the nutritional problems of sub-Saharan Africa means that no firm
conclusion can be reached about the relative nutritional status of males and
females. The companion article [6] explores evidence concerning the determinants
and consequences of the nutritional status of girls and women in sub-Saharan
Africa.

Acknowledgements

The review on which this and its companion article are based
was originally undertaken as part of the work of the Institute of Medicine (IOM)
Committee to Study Female Morbidity and Mortality in sub-Saharan Africa, of
which the first author was a member. We would like to acknowledge the extremely
useful comments and input of the other committee members (Maureen Law [Chair],
Uche Amazigo, Judith Fortney, Philip L. Graitcer, Françoise F. Hamers, H.
Kristian Heggenhougen, Karungari Kiragu, Walinjom F. T. Muna, Jonathan E. Myers,
Benjamin O. Osuntokun, Patience W. Stephens, Judith N. Wasserheit, and Belmont
E. O. Williams) and of the IOM staff who worked with the committee (folly F.
Harrison, Dana Hotra, Delores Sutton, and most especially, Christopher P.
Howson, Project Director).

3. United Nations Administrative Committee on
Coordination/Subcommittee on Nutrition. Second report on the world nutrition
situation. Vol. I. Global and regional results. Geneva: United Nations
Administrative Committee on Coordination/Subcommittee on Nutrition,
1992.

17. Kavishe FP. Analysis of the nutrition situation and trends
in Tanzania during the 1980s. In: Review of nutrition relevant actions in
Tanzania. Report for the United Nations ACC/SCN. Geneva: United Nations
Administrative Committee on Coordination/Subcommittee on Nutrition, February
1992: 27-50.

20. Fakambi LK. Factors affecting the nutritional status of
mothers. The food and nutrition program of the Ouando Horticulture and Nutrition
Center in the Peoples Republic of Benin. Washington, DC: International
Center for Research on Women, June 1990.

Non-privileged women consumed a diet deficient in all nutrients except
iron and thiamine, with an average daily protein and energy intake less
than 60% of FAO/WHO recommendations.

The diet of privileged women met the recommendations for all nutrients
except calcium (45% of recommendations) and vitamin A (95% of recommendations).

Babies of non-privileged women had lower mean birthweights than babies
of privileged women.

Percentage of dietary energy from cereals was 41.2% for privileged and
65.5% for non-privileged women.

Percentage of dietary energy from dairy products, meat, and fish was
22.0% for privileged women and 4.3% for non-privileged women.

Kenya [13]

1984-86

290 rural Embu households

Women progressively lowered their food intake during pregnancy, not only
during times of food shortage, but also during normal years.

Mean weight gain during pregnancy was only 50% of the recommended weight
gain for US or UK women.

Mean birth length was below normal (20th per-centile), and 16% of infants
were considered intrauterine growth-retarded, indicative of maternal malnutrition.

Kenya [48]

1984

Average height of Kenyan children (girls and boys) was that of the lowest
3% in the reference population.

Extent of chronic malnutrition may be partly due to cultural practices,
such as serving food first to the father and other men, next to the first
son and other children according to age, and last to the mother.

Kenya [49]

1983

524 households in Kibwezi

Women had a higher level of stress accompanied by ill health than men.

Women were thinner and shorter than women in other regions of the district.

Prevalence of chronic disability was higher among women than among men,
especially women of child-bearing age.

Mean weights of NBW girls were persistently less than those of NBW boys.

Mean weights of LBW girls were also less than those of LBW boys, but
the mean ratios for boys are less than those for girls; towards the end
of the first year of life the mean ratios converge. The same applies to
length.

Curves for weight and length of NBW and LBW children deviate from the
standard at 18 wk for girls and 12 wk for boys.

Weight curves for LBW children show catch-up growth during the first
months of life, more pronounced in girls than in boys. Later both curves
run a course below the 80% line.

Mean birth length curves for LBW children follow the 90% line for boys
and a slightly higher level for girls.

Mean weights of both LBW and NBW boys lag slightly behind those of girls
at 52 wk.

There was a gradual fall in mean weight-for-height with advancing duration
of pregnancy.

Malawi [32]

1970

Protein-energy malnutrition was very common among pre-school children,
and a striking feature was the general lack of well-being of women, especially
mothers (Dr. A. Burgess, WHO, 1964).

Mozambique [54]

1985

1,060 pregnant women (68% rural) from 10 sites

Women from the North were shorter than women from the South (average
height, 152 and 159 cm, respectively).

Nulliparous women who needed Caesarean section because of cephalopelvic
disproportion were, on average, significantly shorter than controls; 36%
of women who had Caesarean section and 9% of those who delivered vaginally
were <150 cm tall.

Maternal height was also significantly correlated with previous perinatal
loss.

Percentage of women in a site with haemoglobin levels below 90 g/L varied
from 5% to 15%; 1% of all women had haemoglobin levels below 70 g/L.

Main causes of anaemia were found to be iron deficiency and malaria.

Low haematocrit values were associated with small upper arm circumference
and low skinfold thickness, indicating that anaemia was correlated with
undernutrition.

Occasional cases of folic acid deficiency were found among severely anaemic
women.

Rwanda [34]

1965

Prevalence of Bitots spots per 1,000 was 2.6 for women, 13.3 for
men, 3.6 for girls, and 15.4 for boys.

Goitre was more frequent among females than among males in Rwanda and
Burundi.

Sudan [32]

1970

Kwashiorkor and marasmus were both common, perhaps because of the widespread
custom of allowing fathers and older boys to eat first, leaving women
and children to fend for themselves.

Births were markedly seasonal in areas with holendemic malaria, especially
among older women, as a result of physical exhaustion due to food shortage,
heavy work, and anemia, aggravated by a high rate of infection with malaria.

United Republic of Tanzania [55]

1985

Birthweights were higher in urban areas and higher in years of lower
rainfall. Seasonal and yearly variations were in the range of 100-200
g. The magnitude of the variation is comparable to that recorded in famine
conditions, so it is probably significant. The variation is affected by
differences in the food supply, which can cause variations in birthweight
of 50 g.

Seasonal variation was primarily due to the coincidence of seasonal food
shortage and heavy agricultural work.

United Republic of Tanzania [56]

1976

244 pupils, 51% male, mean age 12.5 yr

43 of 117 girls (37%) had weight-for-age between 70% and 80% of standard,
and 31 (26%) had weight-for-age below 70% of standard; 31 of 121 boys
(26%) had weight-for-age between 70% and 80% of standard, and 62 (51%)
had weight-for-age below 70% of standard.

United Republic of Tanzania [32]

1970

In Kisarawe district, 50% of women and 27% of men had clinical signs
of anaemia, which was thought to be a result more of malaria and hookworm
infestation than of nutritional deficiency.

In the same district, 39% of women, 20% of men, and 24% of children were
infested with hookworm.

Zambia [57]

1983

Subjects from recent nutritional status and dietary surveys

Of 572 pregnant and lactating mothers examined, 95.3% had low or deficient
serum albumin levels. Of the same group, 90.5% had high serum globulin
levels.

12% of examined women were deficient and 10.2% had low levels of haemoglobin.

Nearly 2% of the women had deficient retinal or vitamin A levels. 82%
of the women had low retinal levels.

Percentage of wasted females was greater than the percentage of wasted
males. 16.9% of females and 0.0% of males were severely malnourished;
11.9% of females and 6.6% of males were moderately malnourished; 28.9%
of females and 22.0% of males were mildly malnourished.

Zimbabwe [32]

1970

56 of 71 females and 26 of 40 males had goitrous thyroid enlargement.

In a survey of 2 villages (Dewe and Tendenguwo), the total village prevalence
was 74%. 186 of 243 children had goitre (80% of girls and 59% of boys).

In another region (Omay Tribal Trust Land), the highest prevalence of
goitre (77%) occurred among adolescent girls; the prevalence for girls
aged 6-12 yr was 67.9%.

Among 341 patients at Harare Hospital, anaemia was noted in 13.5% of
females and 26.5% of males, due to iron deficiency in 8.3% of females
and 2.7% of males.

Middle Africa

Cameroon [61]

1968

More than 10% of women and slightly more than 5% of men were underweight.

Cameroon [62]

1978

900 children aged 3-59 mo

No consistent relation between sex and the prevalence of undernutrition
was found.

Zaire [63]

1987

Data from various studies in Lemba village, Shaba region, 1975-78

Because of a distinctive form of matrilineal social organization, emphasizing
the social value of women, the Lemba of south-eastern Shaba in Zaire maintain
greater nutritional equality between women and men than do neighbouring
groups with different social organizations and lower status of women.

Zaire [18]

1980-85

118 adult men and 91 adult women, both Efe (foragers) and Lese (farmers)
living in tropical rain forest

Mean height of Lese men was 161.8 cm: among Efe (sometimes known as pygmies),
mean height was 137.1 cm for women and 144.8 cm for men.

Both groups were thin and showed substantial seasonal weight gain and
loss (greater among Lese than Efe): mean BMI of Lese women ranged from
21.9 to 19.8, whereas BMI of Lese men showed a broader range from 22.3
to 19.4

Zaire [64]

1975

Several hundred reproductive-age women and their children followed at
4 Maternal and Child Health clinics in Kiva Province

Highland women and Ntomba women of the equatorial forest had similar
BMIs, but Tembo women of the equatorial forest had lower BMI (19.7).

Seasonal deficiencies of protein and lipids lead to extended post-partum
amenorrhoea among rural highland women: BMI of amenorrhoeic lactating
women was lower than that of menstruating lactating women.

Southern Africa

Lesotho [31]

1971

On the basis of comparisons of their height with Institute of Nutrition
of Central America and Panama (INCAP) standards, girls and boys were similar,
with the majority being at least 1 yr growth-retarded (83% of girls and
85.7% of boys).

71.9% of girls and 74.8% of boys were classified as having grade I malnutrition
or worse according to weight.

Skinfold measurements revealed 66.4% of girls and 63.9% of boys were
below Canadian Standards.

No important differences between boys and girls of any age group were
found for prevalence of goitre, an unusual finding.

South Africa [31]

1971

Of 1,116 children with kwashiorkor, 43 girls and 65 boys had xerophthalmia.

Before supplementation, elderly women were more deficient in riboflavin
than elderly men or adolescents; there were no differences between male
and female adolescents in the prevalence of riboflavin deficiency.

Riboflavin supplements were given for 5 wk during the rainy season when
indicators of riboflavin deficiency increase (and mean weights decrease).
Riboflavin status improved progressively and reached normal values for
both age groups and sexes.

Gambia [12]

1987

197 supplemented and 182 control rural women

Before intervention, women were in positive energy balance during the
dry harvest season, with pregnancy weight gain >1,200 g/mo. In the
wet season, women were in negative energy balance, with pregnancy weight
gain <500 g/mo.

Birthweight was correlated with womens energy balance and averaged
2,944 and 2,808 g in the dry and wet seasons, respectively.

Supplementation was ineffective during the dry season but highly effective
during the wet season.

Girl babies were on average 189 g lighter than boy babies.

Girls had a shorter mean gestation time than boys (37.8 vs 38.3 wk).

Gambia [69]

1982-85

32 pregnant women aged 20-35 yr (primiparous women excluded)

Levels of total energy expenditure ranged from a minimum of 2,300 kcal/d
(1.7 x BMR) in Jan-Mar to a maximum of 2,700 kcal/d (2 x BMR) during the
agricultural season (Jul-Oct).

Pre-supplemented dietary energy intake of pregnant women varied from
an average of only 1,480 kcal/d in the dry season to a minimum of 1,300
kcal/d in the wet season.

In the dry season, women were in positive energy balance (satisfactory
weight gain and deposition of subcutaneous fat).

In the wet season, women were in marked negative energy balance because
of a reduction in energy intake and high energy expenditure.

Maternal protein intakes were not grossly deficient.

Gambia [70]

1978-79

196 women of child-bearing age

Levels of dietary energy intake were low; during the optimum dry season
months, they were only 62% and 64% of the international recommended intake
for pregnant and lactating women, respectively.

Average energy intakes during the dry and wet seasons, respectively,
were 1,483 and 1,417 kcal/d during pregnancy, 1,773 and 1,474 kcal/d during
the 1st trimester of lactation, and 1,662 and 1,413 kcal/d during subsequent
trimesters of lactation.

Pregnant women gained 1.4 kg/mo body weight in the dry season and lost
weight in the wet season. Lactating women gained weight in the dry season
and lost weight in the wet season. Non-pregnant women lost 1.0 kg/mo in
the wet season.

Maternal nutritional status did not deteriorate with increasing parity.

Wet season energy intakes were clearly inadequate.

No maternal depletion in iron, haemoglobin, riboflavin, or vitamins A
and C was noted.

Ghana [22]

1990

Females do not appear to be nutritionally at a disadvantage in Africa
generally or in Ghana specifically.

Levels of acute malnutrition at 6-24 mo of age were appreciably higher
among boys than among girls, for most severe cases as well as more moderate
cases.

Adult men were leaner than women overall, although more women were observed
in the lowest categories.

There was a surprisingly large number of females with BMIs in the higher
brackets, indicating overweight or obesity.

Ghana [71]

1976-77

196 children aged 4-60 mo

There was a slight relationship between sex and nutritional status; boys
tended to be better nourished, even though no preferred treatment for
boys was articulated or observed.

Ghana [72]

1973

3,700 male and female subjects of all ages

There was a drop in mean weight and height compared with standards in
girls at 18-35 mo and in boys at 12-35 mo.

Mean weight-for-age and mean height-for-age as a percentage of standard
were higher in females than in males; the differences between females
and males were greater for weight-for-age; however, all differences between
females and males were very slight.

Mean weight-for-height as a percentage of standard was also higher in
females than in males, except for age 11-16 yr, where values for males
were higher.

Guinea (personal communication, NB Mock and MK Konde, 1991)

1991

913 households

Of 780 women, 11.3% were at a health risk and 12.2% were abnormal according
to BMI. Rural mothers were worse off than urban mothers.

Maternal demographic factors and household activities may have a significant
impact on maternal nutritional status.

Mali [23]

1990

441 adults, 320 women and 121 men, aged 19 yr and older

When compared with National Center for Health Statistics (NCHS) references,
women were less nutritionally disadvantaged than men. Mean height for
women was 160.4 cm (Z score, -0.5) compared with 171.3 cm (Z score, -0.84)
for men. Mean BMI was 20.8 for women and 20.0 for men. No sexual dimorphism
was found in arm circumference, due to heavy physical work done by women
starting at an earlier age than men.

Niger [73]

1980-81

54 nomadic pastoralist families: 30 non-pregnant women and 32 men over
18 yr of age

Marked seasonal variation in weight was seen in both men and women. In
February, at the end of the rainy season, women were on average 87% of
weight-for-height; by May they had lost on average 4.6% of body weight,
declining to 84% of weight-for-height. Men were only 82% of weight-for-height
in February and dropped to 78% by May.

The youngest and shortest women had the highest prevalence of contracted
pelvis and were at greatest risk of developing cephalopelvic disproportion
and of requiring delivery by Caesarean section or embryotomy.

With increasing maternal age and height, rates of these three pregnancy
complications fell.

The tallest women, irrespective of status, rarely had contracted pelvis
or cephalopelvic disproportion.

Nigeria [11]

1985

69 Hausa primigravidae

Early teenagers were enrolled in combinations of antimalarial, folic
acid, and iron supplementation treatment during pregnancy; height was
measured once during pregnancy and once during puerperium (1-60 after
delivery). Height growth ³ 2 cm occurred
among 29% of those in placebo and antimalarial groups and in 71% of those
receiving folate and/or iron supplementation.

Study concluded that protecting young teenage pregnant girls from malaria
and adding nutritional supplements to their diets enhanced maternal and
foetal growth and led to a statistically significant reduction in the
proportion requiring abdominal deliveries (see also ref. 74).

Senegal [62]

1968

More than 65% of children were found to show some sign of nutritional
deficiency, regardless of ethnic group or sex. Anaemia was common, except
among adult men.

Sierra Leone [75]

1978

480 children aged 0-59 mo, 3,724 mothers, 1,965 households

8.2% of mothers were less than 150 cm tall, and 6.1% were undernourished
according to measurements of arm circumference.

Joanne Leslie is with the University of
California, Los Angeles, School of Public Health, Department of Community Health
Sciences, and The Pacific Institute for Womens Health, in Los Angeles,
California, USA. Suzanne Bibi Essama is with the Tulane University School of
Public Health in New Orleans, Louisiana, USA. Elizabeth Ciemins is with the Los
Angeles County Department of Health Services, STD Program, in Los
Angeles.

Abstract

This article reviews existing data concerning the causes
and consequences of female malnutrition in sub-Saharan Africa. As in most parts
of the world, the primary cause of female malnutrition is household food
insecurity compounded by low household and individual incomes. Gender-specific
factors that further undermine womens nutritional status are the severe
physiological burden of frequent child-bearing and the continuous long hours of
energy-intensive work. Negative consequences of malnutrition among females
include high rates of mortality and morbidity, impaired learning, low
birthweights, and reduced energy for discretionary activities. We question the
conclusion of other studies that African women have developed special
adaptive mechanisms to compensate for nutritional deprivation, and
recommend that further research investigate the hidden individual and societal
costs of malnutrition among women.

Major determinants of female
nutritional status

Crucial conflicts face poor women in low-income
countries as they try to fulfil their economic, biological, and social roles at
each stage in the life cycle, particularly during the child-bearing years.
Changes in behaviour that enhance their contribution to one area can have
crucial negative effects on their other roles and activities. This role conflict
relates to the tremendous time, energy, and money-resource constraints facing
these women....

Conflicts between the economic, reproductive, and cultural
roles of women can have detrimental effects on their nutrition and/or that of
their families [1].

The hope in this article and its companion article [2] is that
a first attempt to assemble in one place much of what is known about the
nutritional situation of women and girls in sub-Saharan Africa will lead to
interim recommendations that may be useful to policy makers and programme
planners. Even more, it is hoped that this review will suggest hypotheses and
stimulate interest in conducting multidisciplinary applied research concerning
the extent, causes, and consequences of nutrition-related problems among
sub-Saharan African females throughout their life cycle, and that such research
will, in turn, provide a stronger foundation for the design of appropriate,
cost-effective interventions to improve the nutrition and health situation of
women and girls in this region.

Models of determinants of both childrens and
womens nutritional status standardly include quality and quantity of
dietary intake, infection, and energy expenditure as proximate determinants,
which are themselves seen to be determined by a range of household, community,
national, and global variables related to wealth, food production, education,
and availability of health services, among others [see refs. 3-5]. In
sub-Saharan Africa in particular, women devote enormous amounts of time and
energy to both their productive and their reproductive roles. The time- and
energy-consuming nature of their tasks has significant implications for their
own nutritional status and that of their children.

Womens role in food production and
acquisition

Womens agricultural labour in sub-Saharan Africa is
extremely important both as a percentage of total agricultural labour and as a
percentage of womens total labour force participation. Almost 80% of
economically women in sub-Saharan Africa are working in agriculture [6].
Throughout most of the region, women not only put in longer work days overall
than men [7, 8], but also spend more hours per week in agricultural work [1, 6].
Womens responsibility is at least equal to that of men in determining the
quantity of food available at the household level, and it is significantly more
important in determining the variety and palatability of the household diet [9].
In sub-Saharan Africa, womens dominant role in both subsistence food
production and food preparation may give them more control over their own and
their childrens dietary consumption than in some other regions of the
world; however, this comes at the cost of extremely long and energy-demanding
work days [9-11]. Findings from a study in Malawi of the gender division in
agriculture-related decision-making are not atypical of the region as a whole
[12]. This study found that husbands made most of the decisions regarding major
farm inputs and had almost complete control over decisions concerning cash crop
production. Women had significant input into decisions regarding the production
of food crops, and full responsibility for decisions relative to the cultivation
of selected vegetables, such as pumpkins and beans, that are used in food
preparation. With respect to the use of income, men appeared to have control
over formal, more regular sources of income (i.e., income from the sale of cash
crops or employment), whereas women tended to manage the income from the sale of
beer, fruits, or cooked food items.

An increase in demand for male labour during colonialism may
help explain womens current dominance in agricultural labour. The current
distribution of gender roles is, however, lopsided and asymmetrical. While women
have taken over many of the tasks that were traditionally outside their domain,
such as agricultural labour, men have not done the same in regard to
womens roles [11]. The result has been an inequity in the burden of labour
between men and women and simultaneous declines in womens social and
economic status. Events occurring during colonialism adversely affected women in
several ways. A redistribution of land caused women to lose their limited access
to and ownership of land and their subsequent access to credit, loans, and
technologies. An increase in cash cropping affected women by increasing demand
for their labour. Finally, the imposition of Western notions of womens
inferiority added to their declining status and clashed with African
womens defined independent roles in their societies, which undermined
womens ability to maintain good household nutrition [11,13].

Today, traditional food production and security strategies are
rapidly changing in sub-Saharan Africa in response to population increases,
deteriorating environmental conditions, and changing market circumstances,
resulting in significant urban migration and increased linkages between rural
communities and major urban centres. This adaptation process has led to
significant modifications in food production patterns, in the distribution and
acquisition of food, and in household food consumption. In particular, gender
asymmetries in access to productive resources have meant that women are less
able to take advantage of agricultural intensification strategies in their role
as food producers [11, 14].

Concerns have also been raised about the effects of
agricultural intensification strategies on the health and nutritional well-being
of women and children [11,15, 16]. Some studies have suggested that an expansion
and intensification of commercial agriculture in sub-Saharan Africa has
contributed to gradual declines in food production levels and reductions in the
amount of food available for household consumption. It has also been argued that
women and children may be adversely affected by a shift to cash cropping as a
result of increased demands on womens labour for agricultural activities
and reductions in womens individually earned income, and that children, in
particular, may be adversely affected by earlier weaning and a reduced frequency
of meals during the peak of the agricultural season. Conversely, it has been
argued that a shift to cash cropping has produced higher household incomes that
lead to better household diets and, therefore, to improved nutritional status
for all members of the household, including women and children.

The most rigorous examination of the effects of cash crop
production on child health and nutrition comes from a comparative analysis of
six methodologically similar studies carried out by researchers at the
International Food Policy Research Institute (IFPRI). Four of these studies were
conducted in sub-Saharan Africa (Gambia, Kenya, Malawi, and Rwanda [4]), and the
other two in Guatemala and the Philippines. In the African countries, a
comparison of child outcomes in households that participated in a cash cropping
scheme and those that did not found no evidence of a negative effect of
participation in cash cropping on the nutritional status of children, but only
weak evidence of a positive effect. The comparison with the findings from the
Guatemala study, focusing on a vegetable cooperative, is illuminating. Guatemala
was the only one of the six countries in which household participation in cash
cropping was significantly associated with better child health and nutrition
outcomes. This was attributed to the fact that the vegetable cooperative
directly invested some of its profits in community health and social
services.

Other studies from Africa have reported a negative association
between increased cash cropping and both the quantity and quality of foodstuffs
available for household consumption. Spring [17] presents numerous examples of
the negative effects of increased production of non-food crops and sales of
foodstuffs outside the household. In Zambia, Malawi, and Kenya, cash cropping
resulted in decreased amounts of food available for household consumption, but
whether this resulted in poorer nutritional status was not determined. One
classic example is the introduction of cocoa production in Ghana, which resulted
in a shift of responsibility for the labour-intensive production of yams from
men to women. Unable to cope with their increased workloads, women eventually
switched to producing cassava, which, while requiring less labour, is also less
nutritious and less agriculturally advantageous than yams [18].

Another study from the Gambia, however, reported a situation
in which household nutritional status was positively affected by investments in
technology, despite the fact that women lost control over a crop [19]. Rice, a
crop traditionally controlled by women, was the focus of introduction of new
modes of production. As technology increased, the percentage of rice fields for
which women were responsible declined, which would normally result in reduced
household energy consumption. In this case, however, overall household income
increased, resulting in a significant improvement in the nutritional status of
children and women, especially in the most nutritionally vulnerable households.
The new rice technology also helped to level out seasonal fluctuations of
womens weight, which was particularly beneficial for nutritional status
during the rainy season, when food stores are low and energy expenditure is
high.

A separate analysis of data from a study in Kenya by IFPRI
examined the effects of the commercialization of agriculture on the allocation
of time and the patterns of food consumption by women, as well as on their
nutritional status [20]. The central findings were that women from households
that produced sugar cane spent no more time away from home than women from
households that did not produce sugar cane; that there were no significant
differences in the amount of time spent on the various household activities (as
the amount of time women spent on sugar cane production was negligible); and
that the mean weights of women were similar in households that did or did not
produce sugar cane.

The seasonal patterns of the agricultural cycle in sub-Saharan
Africa impose different demands on womens energy expenditure throughout
the year and have a significant influence on household food availability,
womens energy intake, and womens nutritional status. The periods of
greatest nutritional stress for rural women usually occur during the pre-harvest
period (generally known as the famine or lean months),
when household food stocks are low, the energy demands of agricultural work are
highest, and energy intake is low [9, 10, 12, 21, 22]. In urban areas, periods
of nutritional stress occur when the market prices of basic food commodities are
highest.

The effect of seasonality on womens nutritional status
in sub-Saharan Africa is particularly well illustrated by a study in southern
Benin that compared the effects of seasonal changes in food availability on
womens nutritional status in rural and peri-urban areas [23]. Findings
were reported for a sample of 567 non-pregnant (but lactating) women, of whom
366 lived in rural areas and 201 lived in a pert-urban setting. The findings
concerning seasonality were reported in terms of nutritional status changes
between pre- and post-harvest seasons. Twenty-five percent of the rural women
gained more than 2 kg between the pre- and post-harvest seasons, and the average
body mass index (BMI) also increased significantly during this period. In
contrast, 25% of the pert-urban women lost more than 2 kg during the same time
period and their BMI decreased, although the decrease was not statistically
significant. The Benin study illustrates that the food security and nutritional
consequences of seasonal changes in food availability can differ significantly
between rural women (who depend mostly on food from their own production) and
pert-urban women (who obtain a large proportion of their food through
purchase).

Pregnancy and lactation

With an average regional fertility rate of 6.5% in 1990, women
in sub-Saharan Africa had significantly higher fertility than women in any other
region of the world [24]. Studies of food consumption during pregnancy and
lactation in sub-Saharan African countries indicate that macronutrient intakes
are low, in the range of 1,400 to 2,000 kcal and 25 to 50 g protein per day,
while vitamin and mineral intakes are often extremely low [1, 25]. Although this
low dietary intake clearly carries risks for both mothers and infants, several
detailed studies suggest that when the energy cost of activity, reproduction,
and lactation can be partially met by mobilization of maternal tissue stores,
the impact of low energy intake on foetal growth and lactation performance is
less than might be anticipated [26]. Other studies, however, emphasize that
since lactation has even higher energy requirements than pregnancy, it is
essential to increase energy intake, reduce energy expenditure, or both during
breastfeeding to protect womens long-term nutritional status
[27].

Kosin et al. [28] analysed cross-sectional data on food
consumption in Machakos area, Kenya, by pregnant, non-pregnant, and lactating
women from October 1977 to December 1979, and found that the diets of pregnant
women, and to a lesser extent those of lactating women, were inadequate both
when compared with the intakes recommended by the World Health Organization
(WHO), and when compared with the diets of non-pregnant, non-lactating women in
the same population. Compared with the recommended daily intakes, pregnant women
received adequate amounts of protein, thiamine, and ascorbic acid. However,
their energy intakes were low, with median values ranging from 70% of
recommended intake during the first trimester to 62% during the third trimester.
An even larger deficit was recorded in the median calcium, iron, retinol
equivalents, and riboflavin intakes of pregnant women. Kosin could not explain
clearly why food intake was reduced in the last trimester of pregnancy and
suggested that cultural factors could be major determinants, as food
availability was not a constraint in that region. The dietary intake of
lactating women was found to be inadequate in energy and in all nutrients except
protein and ascorbic acid. However, the deficits noted were lower than the
deficits found among pregnant women. The study found that mean weights remained
the same during the first and second trimesters of pregnancy and were only 2 kg
higher in the third trimester. The mean weight-for-height of lactating women at
15 to 24 months was slightly lower than the mean for women during the first year
of lactation. The authors concluded that the nutritional status of Kenyan women
deteriorated as pregnancy and lactation progressed.

Studies of European and American women report significant
increases in skinfold thickness at triceps and subscapular sites of the body
between 10 and 20 weeks of pregnancy. Comparable analyses of changes in skinfold
thickness at various stages of pregnancy in Africa are rare. A study of pregnant
Nigerian women is one of the few published studies on the subject [29]. It
provides an excellent analysis of the magnitude and patterns of subcutaneous fat
deposition at triceps and subscapular sites in a group of normal
pregnant Yoruba women living under low socioeconomic conditions in rural areas.
All the women in the study had had multiple pregnancies. Their mean age was 27
years, and on average each woman had completed four pregnancies at the time of
the study. Other anthropometric measurements collected on the women included arm
circumference, weight, height, age, and parity number. Like the Kenyan study
described above and other research from sub-Saharan Africa, this study found low
weight gains during pregnancy. The total mean weight gain between 20 and 30
weeks of pregnancy was 3.8 kg, which was about half of that reported for elite
Nigerian women in Ibadan. The study also reported gradual declines in arm
circumference and in triceps and subscapular skinfold thickness throughout
pregnancy; the average total decline for the whole group was 4.1 mm. Thus,
instead of showing a normal increase between 20 and 30 weeks of pregnancy, both
individual and combined skinfold thickness at the triceps and subscapular sites
of low-income pregnant Nigerian women declined. The authors interpret these
declines as indicating a continuous depletion of the energy stores during the
course of pregnancy to compensate for inadequate dietary intake. In addition,
the study found a negative correlation between parity and subscapular skinfold
thickness, which was interpreted as indicating that the ability of pregnant
women to store body fat at the subscapular site decreased as parity
increased.

There is mixed evidence concerning the extent to which women
are actually able to reduce energy expenditure to compensate for the increased
energy demands of pregnancy or lactation. Most research has found little
evidence of a change in activity patterns or energy expenditure during pregnancy
or lactation by women in sub-Saharan Africa or elsewhere in the developing world
[12, 30]. However, a recent detailed study of the functional consequences of
malnutrition among the Embu in Kenya found that reduction in energy expenditure
during the third trimester was a major mechanism by which pregnant women were
able to achieve reasonable infant birthweights in the face of inadequate dietary
intake [31]. Evidence of the contribution of energy-sparing mechanisms to
partially meet the additional energy demands of pregnancy also emerges from a
series of studies of women in three rural Gambian villages. The energy
expenditure of pregnant women on activities with relatively low energy demands
did not appear to change over the course of pregnancy, whereas activities with
higher energy demands were reduced during the second and third trimesters
[3234]. Peacock and colleagues [35] reported a similar finding of a reduction in
energy-intensive activities in one, but not both, of the Zairian tribal groups
they studied. Among Efe women (semi-nomadic foragers), the proportion of time
spent in the most energy-intensive activities was reduced during pregnancy and
even more during lactation. However, no compensatory reduction in energy
expenditure was found among pregnant or lactating Lese women, who work as
swidden cultivators.

The general problem of meeting the nutritional demands of
pregnancy and lactation on top of the already substantial energy demands of a
long and physically demanding workday is particularly acute during seasonal
periods of food shortage. This is well illustrated by the Gambian research
referred to above. Fifty women subsistence farmers were followed through
pregnancy, during which time some were provided with food supplements, and
seasonal changes in basal metabolic rate, body fat, activity patterns, and total
energy expenditure were assessed [36]. Seasonal variations in body-fat content
were found to occur in all women, whether pregnant or not, and fat gain during
pregnancy in individual women was found to be dependent upon the times of the
year through which the pregnancy progressed. Seasonal fluctuations in body-fat
content of rural Gambian women were as large as, or larger than, the changes
resulting from pregnancy. Weight loss during the rainy season among
unsupplemented non-pregnant, non-lactating women averaged 5 kg, most of which
was adipose tissue. Among pregnant women, unsupplemented women who gave birth at
the end of the rains (when agricultural activity was intense and food supplies
were very low) lost 4.7 kg of body fat, whereas those who were pregnant during
the dry season (when little agricultural work was done and food supplies
increased) gained as much as 3 kg of body fat. The interaction between
seasonality and supplementation was highly significant. In supplemented women,
neither weight nor fat gain during pregnancy varied as much with season as in
the unsupplemented group. Overall, supplementation increased fat gain during
pregnancy by about 2 kg and gave some protection against seasonal weight loss.
The authors interpreted their combined findings concerning changes in basal
metabolic rate, fat deposition, and energy expenditure as demonstrating that
maternal nutritional status in rural Gambian women is significantly compromised
by pregnancy during the rainy season.

Given the marginal food availability in most of rural
sub-Saharan Africa, and the need for women to continue with heavy physical work
throughout most, if not all, of the time they are pregnant and lactating, the
importance of ensuring an adequate interval after the end of lactation and
before the next pregnancy to replenish maternal reserves of fat and other
nutrients cannot be overemphasized. It is estimated, for example, that even when
food intake is adequate, it may take two years to replenish body iron stores
after a pregnancy [37]. In addition, efforts to reduce the energy demands on
women during the preconception period, as well as during pregnancy and
lactation, through easier access to needed resources, labour-saving devices, or
both would be extremely beneficial in protecting the health of both women and
children.

Functional consequences: Taking a
life-cycle perspective

Malnutrition is multifactorial in its aetiology and cumulative
in its manifestations. Merchant and Kurz [ref. 3, p. 73] note succinctly that
A nutritional problem is generally the consequence of earlier problems and
the cause of later problems. Some of the most important functional
consequences of female malnutrition (for example, the obstetrical risks
associated with short stature and iron-deficiency anaemia) have been studied
directly in sub-Saharan African populations. Many other functional consequences
of nutritional status (both positive and negative) have not been studied to any
great extent among sub-Saharan African females directly, but reasonable
extrapolations can be made based on studies of men or studies from other parts
of the world.

Mortality and morbidity

The ultimate consequence of severe malnutrition is death.
Malnutrition is a particularly significant contributing cause of infant and
child mortality and of maternal mortality. On the basis of estimates made by
UNICEF and others, it seems likely that at least a third of infant and child
deaths in sub-Saharan Africa are partially attributable to protein-energy
malnutrition [38]. And, in times of famine, both the rates of infant and child
mortality and the proportion of total deaths attributable to malnutrition
increase dramatically [39].

Low birthweight, which can be due to either prematurity or
intrauterine growth retardation, is the most significant nutritional risk factor
for subsequent infant and child mortality. It has been estimated that maternal
nutritional factors account for approximately half the influence of established
determinants of intrauterine growth retardation in developing countries [40].
Current or past maternal malnutrition, as evidenced by short stature, low
weight-for-height, poor-quality dietary intake, or excessive energy expenditure,
is a significant risk factor for bearing infants of low birthweight, showing a
direct intergenerational transmission of malnutrition.

Stunting and wasting among pre-school-age children, whether
attributable to low birthweight or to poor diet and disease, significantly
increase the risk of death. A study in Iringa, Tanzania, for example, found a
sharp increase in mortality risk at weight-for-age below 60% of the median,
weight-for-height below 70% of the median, and height-forage below 85% of the
median [41]. Extensive work by Pelletier and his colleagues at Cornell
University has clearly established that both severe and mild-to-moderate
malnutrition contribute more significantly to child mortality than previously
recognized. For example, from eight community-based prospective studies of the
relationship between anthropometry and child mortality (including studies from
Malawi and Tanzania), they conclude that the relative risk is 8.4 for severe
malnutrition, 4.6 for moderate malnutrition, and 2.5 for mild malnutrition [42].
The finding of an increased mortality risk even among mildly to moderately
malnourished children has important programmatic and policy implications, given
the much larger number of such children compared with those who are severely
malnourished.

After infants and pre-school-age children, those most at risk
of mortality associated with malnutrition are women during pregnancy and
childbirth. Given the extremely high rates of maternal mortality in sub-Saharan
Africa [see ref. 2, table 1], assessing and reducing as many of the major causes
of maternal deaths as possible will be a particularly important component of
improving womens health in this region.

Obstructed labour and its sequelae are the most important
causes of maternal death in sub-Saharan Africa [43]. The risk of obstructed
labour, in which the birth canal is too small or too deformed to allow passage
of the baby, is directly related to maternal age, developmental stage, and
stature. The growth of the birth canal is not complete until about three years
after height growth ceases, and protein-energy malnutrition both slows down the
rate at which girls mature and, in many cases, permanently stunts their growth.
Thus, protein-energy malnutrition directly increases the risk of obstructed
labour, particularly among adolescent mothers. A study in Nigeria found that
among a group of primigravidae who received prenatal care, the proportion who
required operative delivery because of a small pelvis ranged from 40% among
women under 145 cm tall, to 14% among those at least 150 cm tall, to less than
1% among those at least 160 cm tall [44]. A population-based case-control study
in Harare, Zimbabwe, reported similar findings. When other factors were
controlled, women of short stature (less than 160 cm) were twice as likely as
taller women to have an operative delivery (Caesarean section, vacuum
extraction, or forceps) because of cephalopelvic disproportion [45]. Given the
relatively low rate of stunting among women in sub-Saharan Africa compared with
other regions of the developing world, the importance of obstructed labour as a
cause of maternal mortality may seem somewhat surprising. However, the
proportion of births in sub-Saharan Africa occurring among young mothers who are
not yet fully physically mature is part of the explanation. Even more
significant is the widespread lack of access to timely medical intervention when
obstructed labour does occur.

The other nutritional deficiency that significantly increases
the risk of maternal mortality is anaemia. When anaemia is acute, it can cause
death directly from heart failure or shock. Fortunately, even among malnourished
women, anaemia this severe is quite rare. However, although less severe anaemia
may not be a direct cause of maternal death, it is a significant contributory
cause. In particular, anaemic women are less able to tolerate haemorrhage (both
antepartum and post-partum), which is one of the four leading causes of maternal
death in sub-Saharan Africa [43]. Anaemia is estimated to account for a fifth to
a tenth of all maternal deaths in many countries of the region, and in the
extreme circumstances of two refugee camps in Somalia, more than 90% of maternal
deaths were associated with anaemia [37]. Again, however, it is probably more
accurate to say that it is the combination of pre-existing anaemia, haemorrhage,
and lack of access to medical care that causes women to die.

Scientific studies relating malnutrition to both infectious
and non-communicable diseases have proliferated over the past decade. A large
number of micronutrient deficiencies have been found to impair the function of
the immune system, particularly through their effect on cellular immunity [46,
47]. The negative effect of zinc deficiency on the immune system seems to be
particularly notable. As far as non-communicable diseases are concerned, the
effect of malnutrition is cumulative and primarily manifests itself in disease
outcomes during the post-reproductive years. Obesity, and probably excess
dietary fat, are risk factors for both diabetes and coronary heart disease,
whereas low consumption of the antioxidant vitamins A, E, and C increases the
risk of developing most, if not all, cancers [48, 49].

Although the negative effect of specific nutrient deficiencies
on the effectiveness of the immune system has been demonstrated, the functional
significance of this in terms of increased morbidity is less well established.
The largest body of scientific evidence concerns the relationship between
protein-energy malnutrition and diarrhoea. Although virtually all studies show a
strong association between these two widespread health problems of childhood,
the direction of causality has been more difficult to establish. Careful
longitudinal studies suggest that pre-existing protein-energy malnutrition has a
limited effect on the incidence of diarrhoea but significantly increases the
duration [50, 51]. A study of more than 300 children between 6 and 32 months of
age in northern Nigeria at the end of the rainy season found that diarrhoea
lasted 37% longer in stunted children and 79% longer in wasted children; in this
particular study, wasted children also had diarrhoea more frequently
[52].

A longitudinal study of the functional consequences of
malnutrition in the Embu district of Kenya produced several important findings
concerning the relationship between nutritional deficiency and subsequent
morbidity, not only among preschool-age children, but also among reproductive
age women [31]. In fact, one of the most striking results of the research was
the finding that morbidity rates for the study sample as a whole doubled during
the drought-related food shortage period in 1984 compared with 1985, when
dietary intake had returned to more normal levels.

The same research found that stunting among toddlers (18 to 30
months) and, to a lesser extent, low weight-for-age significantly increased the
risk of acute lower respiratory tract infections [31]. There were also
significant sex differences. The percentage of time that female infants and
toddlers spent ill was somewhat higher than for boys (47% versus 42%), and girls
were found to have a duration of severe illness that was, on average, twice as
long as that for boys. Girls also had an energy deficit during severe illness
that was more than double that of boys, although this was somewhat balanced by a
larger food intake during convalescence. Lagged analysis showed improved quality
and quantity of food intake to be protective against severe illness among girls
and boys, with both incidence and duration being affected. In terms of
life-cycle effects of malnutrition, a particularly notable finding of the Embu
study was that lower rates of maternal illness and higher maternal fat intakes
were both significant predictors of less morbidity among their toddlers. The
researchers interpreted both factors as indicative of higher levels of energy
among mothers, who would then be better able to prevent or treat their
childrens illness.

Morbidity rates among reproductive-age Embu women were
significantly higher among pregnant women than among non-pregnant women [31]. In
addition to the well-established negative effects of pregnancy on the immune
system, the researchers attributed the greater morbidity among pregnant women to
their lower food intake. As with toddlers, among both pregnant and non-pregnant
women, higher levels of food intake (particularly total energy, fat, and animal
protein) were found to be protective against severe illness. Overall, women in
this study were found to have higher illness rates than men, a difference that
persisted even when pregnant women were excluded from the comparison. However,
the authors caution that since women were the main informants, male illness may
have been underreported.

Cognitive development and school performance

One of the clearest intergenerational effects of female
malnutrition is the significant level of cretinism, deafness, and other
congenital abnormalities among infants born to mothers who are severely iodine
deficient. Endemic cretinism is estimated to affect up to 10% of the population
living in severely iodine-deficient areas [53]. There are pockets of severe
iodine deficiency in a majority of sub-Saharan African countries; in the region
as a whole, there are estimated to be at least 500,000 overt cretins due to
maternal iodine deficiency during pregnancy [48]. In addition to congenital
cretinism, children who suffer from iodine deficiency during their pre-school or
school years also show delayed mental development, although unlike cretinism,
these cognitive impairments can be reduced with appropriate nutritional
intervention.

Protein-energy malnutrition in children is also strongly
associated with impaired motor and mental development [38, 54]. The effects
appear to be both direct and indirect. A child who is malnourished is often
apathetic or irritable and thus tends to receive less attention and positive
stimulation than a better-nourished child in a similar environment.
Protein-energy malnutrition is negatively associated both with the likelihood
that children will go to school and with how well they are able to learn in
school [55].

The study of functional consequences of malnutrition among the
Embu in Kenya discussed above found negative effects of malnutrition on
cognitive development among both toddlers and school-age children [31]. In both
age groups, stunted children were found to do less well on cognitive tests than
children with normal height-for-age when other factors were controlled. Better
dietary quality, particularly an increased intake of animal protein, fat, and
several micronutrients (including but not limited to iodine), was found to have
a significant positive effect on cognitive development. In addition, current
activity level was strongly related to concurrent energy intake, and activity
level and exploratory behaviour were found to be positively linked to learning
among school-age children.

There are very few studies, in sub-Saharan Africa or
elsewhere, of the effect of malnutrition on attendance, repetition, or drop-out
rates among school-age children, although it is virtually inevitable that a high
prevalence of malnutrition or other health problems among school-age children
will make them inefficient users of the educational resources
available to them [55]. A detailed study of health and nutrition problems among
school-age Yorubu children in Nigeria documents a high proportion of children
going to school without breakfast and a high prevalence of growth retardation
and micronutrient deficiencies. The study concludes that these lead to a high
drop-out rate, poor intellectual performance, and low educational attainment,
representing a serious economic loss to the government of Nigeria, which spends
one-fourth of its annual recurrent budget on primary-school education
[56].

The life-cycle consequences of malnutrition are also well
illustrated by the linkages between malnutrition and schooling. Malnutrition
during the preschool and school-age years has negative effects on girls
(as well as boys) school participation and performance. Low levels of
maternal education are in turn significantly associated with poor child
nutritional status, as well as with higher levels of child mortality
[57].

Reproductive function

The functional consequences of childhood malnutrition
discussed above affect both males and females, although the long-term
consequences may be different, and in some cases more severe, among females.
However, the detrimental effect of malnutrition on reproductive function is
specific to females (with the possible exception of effects of severe
malnutrition on male fertility) and has grave life-cycle and intergenerational
consequences.

Significant declines in fertility during famine, as well as a
predictable return to previous levels of fertility once the famine is over, have
been well documented [58]. Frisch [59] has developed a comprehensive model
relating female malnutrition to a shorter and less efficient reproductive span
through delayed menarche, reduced fecundity, lengthened post-partum amenorrhoea,
and perhaps earlier menopause. Nonetheless, there remains considerable debate
about the magnitude of any effects of female malnutrition on fertility in the
chronically mildly to moderately malnourished populations of sub-Saharan Africa.
An analysis of data from unrelated nutrition and fertility surveys in Senegal,
for example, found evidence of, at most, a minor negative effect of malnutrition
on fertility [60]. Two studies from Zaire, however, have reached conclusions
that suggest a much more significant effect of nutritional status on fertility.
Caraëls [61] analysis of data on lactation status and duration of
post-partum amenorrhoea among women from two different ecological zones of Zaire
found a strong relationship between birth intervals and nutritional patterns.
Although the study did not have individual-level dietary intake data, the
researchers concluded that when duration of lactation was controlled, severe
seasonal inadequacies of protein and lipids prolonged postpartum amenorrhoea
seven to nine months among rural highland women. Even more compelling evidence
comes from a more recent study in Zaire. Women living in different ecological
zones were compared, but in this case the researchers were able to relate
longitudinal anthropometric data and salivary measures of steroids (indicating
ovarian function) with seasonal variations in conception. They concluded
that

Variability in the seasonal pattern of rainfall in
the Ituri Forest causes variability in Lese garden size, which translates into
significant changes in nutritional status. Declines in female nutritional status
result in reduced ovarian function, which produces seasonal reductions in rates
of conception and implantation [ref. 22, pp. 404-5].

Despite widespread mild to moderate malnutrition, women in
sub-Saharan Africa achieve quite high overall levels of fertility. Even more
surprising, perhaps, is the fact that sub-Saharan African women produce infants
with reasonably adequate birth-weights and successfully breastfeed, despite low
energy intakes during pregnancy and lactation (in the range of 1,300 to 1,700
kcal) and a much lower weight gain during pregnancy (7 to 8 kg) than is
recommended or observed among pregnant women in industrialized countries [1,
62]. Part of the explanation for this is the high rate of foetal wastage and
maternal and infant mortality; in sub-Saharan Africa, the most malnourished
foetuses, infants, and mothers simply do not survive.

Some researchers have hypothesized, in addition, an unusual
capacity on the part of pregnant and lactating African women to adjust to or
compensate for low food intake, but the findings are not consistent. A series of
studies in the Gambia, for example, led to the conclusion that women are able to
produce adequate-birthweight infants and adequate amounts of breastmilk by
mobilizing rather than building up fat stores during pregnancy, particularly
during the wet season, and by achieving considerably greater metabolic
efficiency than women in industrialized countries [32, 63]. In particular,
researchers in the Gambia reported that women raised their basal metabolic rates
so little during pregnancy that the net extra cost of basal metabolism was only
1,000 kcal, rather than the usual estimate of 36,000 kcal, over the course of a
pregnancy [33]. These findings are not entirely supported by the results of a
longitudinal study of reproduction among Embu women in Kenya [31]. The Kenyan
research also reports surprisingly good infant birthweight outcomes, in spite of
low energy intake during pregnancy and a weight gain during pregnancy only half
of what is recommended. However, in contrast with the reported findings from the
Gambia, the Kenyan study found no compensatory lowering of resting energy
expenditure among pregnant women. Instead, the researchers found a compensatory
behavioural adaptation: late in pregnancy, women doubled their inactive time (at
the expense of household care, child care, economic and agricultural activities,
and food preparation) in order to accommodate to their low energy intakes
relative to the energy requirements at this stage of pregnancy. In addition, the
study found that as in industrialized countries, pre-pregnancy maternal size,
energy intake during pregnancy, and pregnancy weight gain were all important
determinants of infant birthweight and of net post-partum maternal weight and
fat gain.

Physical work capacity

Both the long-term consequences of childhood malnutrition and
current nutritional deficiencies may have significant effects on womens
capacity for physical work. Given the strenuous nature of the major tasks of
rural women in sub-Saharan Africa - pounding grain, carrying water and fuel,
doing non-mechanized agricultural work, and walking to and from markets - a
womans physical capacity for work may be one of the most important
determinants of her own and her familys nutritional well-being
[5].

In attempting to assess the effects of female malnutrition on
physical work capacity, considerable extrapolation must be done from studies of
males, since surprisingly little research has been done on women. The long-term
effects of childhood malnutrition, acting through short stature and reduced
muscle mass, have a reasonably clear negative effect on the productivity of men
engaged in strenuous activities such as cutting cane or moving earth [64]. In
addition, deficiencies of several micronutrients, particularly iron, but also
vitamin C and the B-complex vitamins, have been found to have a negative effect
on physical work capacity [46]. Intervention studies in which anaemic female tea
pickers in Asia were given supplemental iron showed that those who were
supplemented were significantly more productive than unsupplemented controls
[5].

There is less consistency in studies that have tried to assess
the association between energy status and physical work capacity, in part
because a frequent initial response to inadequate energy intake is to mobilize
fat stores rather than to reduce work [38]. One study from Kenya did find a
positive association between nutritional status and work capacity among women in
sugar cane-farming households [65]. Women of higher BMI were able to spend more
time in work-related activities, including home production, and at a given level
of BMI, taller women appeared to engage in more energy-intensive work
activities. In addition, the frequently cited report from researchers in the
Gambia of women who received a dietary supplement and then sang while they
worked in the fields (which they had not done previously) supports the
importance of looking beyond physical capacity for work or labour productivity
when assessing the functional consequences of adult malnutrition [66].

Conclusion

The main cause of malnutrition of females in sub-Saharan
Africa is the same as for males: household food insecurity due to unreliable
food availability, compounded by extremely low, and for the most part falling,
incomes. The individual nutritional status of both males and females in
sub-Saharan Africa is further undermined by the continuing high burden of
infectious disease in this region, which is particularly significant as a
determinant of childrens nutritional status. Additional important causes
of poor nutritional status among adult women in sub-Saharan Africa are the high
physiological burden of reproduction and the long hours of energy-intensive work
of most rural women in this region.

Female malnutrition in sub-Saharan Africa is responsible for a
broad range of both short-term and long-term negative consequences. As a result
of malnutrition, girls (like boys) suffer high levels of mortality and stunting
in early childhood and poor school performance in later childhood. Malnutrition
among adult women poses severe risks both to themselves and to their infants.
Although stunting is not as widespread among women in most sub-Saharan African
countries as in the rest of the developing world, the lack of access to timely
medical intervention for cephalopelvic disproportion and prolonged labour puts
women with inadequate pelvic development (whether due to size, age, or both) at
extremely high risk. In addition, the high proportion of low-birthweight infants
in many sub-Saharan African countries is substantially attributable to maternal
malnutrition, both before and during pregnancy.

Although some researchers have suggested that sub-Saharan
African women seem to accommodate remarkably well to inadequate food
intakes, multiple pregnancies, long duration of breastfeeding, and long hours of
energy-intensive domestic and market work, such a positive conclusion seems
unwarranted. First, the extremely high infant, child, and maternal mortality
rates and the short life expectancy in sub-Saharan Africa suggest that women and
children who are severely malnourished in this region simply fail to survive,
undoubtedly in part because of the high prevalence of infectious diseases and
the lack of access to medical care. Even among those who survive, however, it
seems almost certain that their marginal nutritional status severely restricts
the energy that girls and women have for any activities beyond those that are
essential for survival. It may turn out that this restriction on discretionary
activities is most responsible for the perpetuation of malnutrition from one
generation to the next and, therefore, that interventions to reduce female
malnutrition could be one of the most effective investments that could be made
in social and economic development in sub-Saharan Africa.

Acknowledgements

The review on which this and its companion article are based
was originally undertaken as part of the work of the Institute of Medicine (IOM)
Committee to Study Female Morbidity and Mortality in sub-Saharan Africa, of
which the first author was a member. We would like to acknowledge the extremely
useful comments and input of the other committee members (Maureen Law [Chair],
Uche Amazigo, Judith Fortney, Philip L. Graitcer, Françoise F. Hamers, H.
Kristian Heggenhougen, Karungari Kiragu, Walinjom F. T. Muna, Jonathan E. Myers,
Benjamin O. Osuntokun, Patience W. Stephens, Judith N. Wasserheit, and Belmont
E. O. Williams) and of the IOM staff who worked with the committee (folly F.
Harrison, Dana Hotra, Delores Sutton, and most especially, Christopher P.
Howson, Project Director).

23. Fakambi LK. Factors affecting the nutritional status of
mothers. The food and nutrition program of the Ouando horticulture and nutrition
center in the Peoples Republic of Benin. Washington, DC: International
Center for Research on Women, June 1990.

24. World Bank. World development report 1992: development and
the environment. Washington, DC: World Bank, 1992.

48. United Nations Administrative Committee on
Coordination/Subcommittee on Nutrition. Second report on the world nutrition
situation. Vol. I. Global and regional results. Geneva: United Nations
Administrative Committee on Coordination/Subcommittee on Nutrition,
1992.

The authors are with the Child Health Department,
National Research Center, in Dokki, Giza, Egypt. Iman Hakim is currently a
Visiting Assistant Professor in the Department of Family and Community Medicine
at the College of Medicine, University of Arizona, in Tucson, Arizona,
USA.

Abstract

High serum cholesterol is a major risk factor for
atherosclerosis. This cross-sectional study (n = 102) investigated the
levels of total cholesterol (TC) and triglycerides (TG) in Egyptian girls aged
11 to 16 years attending a middle-class public school. The mean TC level was
194.27 ± 21.97 mg/dl, and 33.33% of girls had TC levels > 200 mg/dl. The
mean TG level was 160.07 ± 30.83 mg/dl, with 3.92% of the girls showing TG
levels > 200 mg/dl. Most of the girls (65.69%) were overweight, with body
mass index (BMI) >25. Univariate analyses revealed an association of TC and
TG with all anthropometric measures. Using stepwise regression analyses, the
best model for prediction of TC was with BMI and central body fat (explaining
24.76% of TC variance); the final model for TG was with BMI, central body fat,
and abdominal skinfold thickness (explaining 47.49% of TG variance). Our data
show that these adolescent Egyptian girls were heavier and had higher blood
lipid concentrations than subjects in the Bogalusa study and other studies
worldwide. Further studies are needed to determine the factors associated with
these higher lipid levels and to develop appropriate intervention
programmes.

Introduction

Findings of epidemiological, family-genetic, and autopsy
studies have demonstrated that the atherosclerotic process starts in childhood
and further develops in adolescence and early adulthood [1, 2]. One of the most
notable components of the atherosclerotic plaque is cholesterol, both in the
cells and within the matrix of the arterial tissue [3]. Many paediatric
epidemiological studies have demonstrated that blood lipid levels maintain their
relative rank order over time, and therefore high levels in adulthood can be
linked to high levels in childhood [4-8].

Epidemiological and clinical data point to a possible relation
between moderate obesity and premature atherosclerosis. The relationship is
stronger with truncal obesity than with fat deposition in the hips or limbs
[9-12]. Adolescence is a period of rapid growth, sexual maturation, and
emotional, behavioural, and social changes, all of which can have an effect on
blood lipids. Evaluation of body-fat distribution in children and adolescents
may help to identify persons most susceptible to cardiovascular risk in
adulthood [13].

No representative studies on lipids in adolescent girls have
been performed in Egypt. Guidelines of the American Heart Association, the
American Academy of Pediatrics [14], and the United States National Cholesterol
Education Program [15] give the following cut-off points for classifying
children and adolescents (1 to 19 years of age) at risk for high blood
cholesterol concentrations: 170 to 185 mg%, slightly elevated risk; >185 mg%,
high risk.

We report the findings of our recent study on total
cholesterol (TC) and triglyceride (TG) levels in middle-class adolescent
Egyptian girls, relating them to anthropometric factors.

Subjects and methods

Study population

The study population was enrolled in a public middle school
for girls in a middle-class neighbourhood in Giza, Egypt. It was considered
representative of the middle social class. Approximately 550 girls (ages 11 to
16) were enrolled in grades 6 to 8. A 20% sample was drawn from each of the five
classes per grade, and these girls were interviewed (n = 124). Consent
forms were sent to parents asking permission to draw blood. This report
concentrates on cholesterol and TG concentrations in 102 girls with a complete
blood picture and biochemistry.

Determination of lipid profile

Venous blood samples were collected from each girl after an
overnight fast, and concentrations of serum TC and TG were measured with the
Boehringer-Mannheim Diagnostic Analysis Kit. Double quality controls were
performed and revealed a coefficient of analytical variation of 1.2% for TC and
3.2% for TG.

Weight (to the nearest 0.1 kg) and height (to the nearest 0.5
cm) were measured on a balance beam scale with the girls wearing an examining
gown over their underclothing and without shoes. All other anthropometric
measurements were obtained as described by Steinkamp et al. [16, 17], all on the
right side of the body. Measurements were carried out by one graduate student
who had been trained for six months. The mean of three readings was calculated
and used in the analysis. Derived data were calculated as follows: Body mass
index (BMI) = weight/height squared (kg/m2). Body build = chest
circumference/height [18]. Body-fat distribution: upper-lower fat pattern = arm
circumference/thigh circumference [19]; central-peripheral fat pattern =
subscapular skinfold/triceps skinfold [19]; waist-to-hip ratio (WHR) = waist
circumference/hip circumference [16, 17]. The arm-to-thigh ratio measures the
relative distribution of upper versus lower peripheral body fat. The
subscapular-to-triceps ratio measures the relative distribution of central
versus peripheral upper body fat.

Data analysis

Means, standard deviations, and ranges were calculated for
each study variable. Pearson correlation coefficients were calculated among all
independent variables and between each independent variable and each of the
serum lipids (TC and TG).

To test the relative contribution of selected study variables
to the variability of each lipid level, a multiple linear regression was
performed followed by a stepwise variable selection procedure. In this analysis,
we first seek the linear combination of anthropometric factors and lipid levels
(TC and TG) that has the maximum correlation.

The independent variables in the regression procedure were
potential correlates of each lipid level and were selected to minimize
multicolinearity, or interdependence, so that two variables did not describe the
same phenomenon. That is, if a high degree of association was found between two
variables describing a similar phenomenon, only one would be entered in the
stepwise model. Only variables selected as most potent from the preceding
correlation analysis were treated as independent variables in a stepwise
multiple regression. This method allowed us to determine the order of importance
of each anthropometric variable for describing or predicting TC and TG. Only
subjects with data available on every study variable were used in the stepwise
regression analysis.

Statistical analyses were performed using the statistical
package Stata [20] at the University of Arizona, Tucson. Two-sided p values
<.05 were considered significant.

Results

Table 1 shows the distribution of the anthropometric
measurements and lipid profiles for the study population. Most of the girls
(66%) had BMI >25.

The distribution of the girls TC and TG levels is shown
in figures 1 and 2. The mean TC and TG values of all girls were 194 ± 22
mg/dl and 160 ± 31, respectively. The percentages of TC and TG levels in
various ranges are shown in table 2. Seventy-seven percent of the girls had TC
levels greater than 185 mg/dl, and 22% had TG levels greater than 185 mg/dl.
Thirty-four percent had TC levels greater than 200 mg/dl, and 4% had TG levels
greater than 200 mg/dl.

A worldwide review [21-26] of TC and TG levels in adolescent
girls in the last 20 years (table 3) allowed us to compare our results with
those of other studies in different countries. The mean serum TC level in the
adolescent Egyptian girls exceeded the levels in the Bogalusa study and other
American reports by more than 15 mg/dl.

Univariate analysis

Pearson correlation coefficients between the various study
variables and serum TC and TG are given in table 4. The findings show that
neither TC nor TG was associated with age or pubertal stage. On the other hand,
both TC and TG were significantly associated with all anthropometric measures
except for height, span, and upper fat pattern. In addition, TC was not
associated with either biceps skinfold thickness or WHR, and sitting height was
not associated with TG.

Regression analyses were then performed to evaluate the effect
of several factors simultaneously and to quantitate the relative contribution of
each variable to serum lipids when examined in the presence of all other study
variables. Only those variables considered significant at the univariate level
were considered as potential variables for entry, i.e., BMI; suprailiac,
femoral, and abdominal skinfold thicknesses; central fat pattern (triceps
skinfold/subscapular skinfold); waist and thigh circumferences; and
WHR.

The results of the final model are shown in table 5. Two
variables entered the model as significant predictors of TC level: BMI and
central body-fat pattern. These two explained 25% of the variance in TC level.
TG level was best predicted by BMI, central body-fat pattern, and abdominal
skinfold thickness, which explained 48% of the variance.

Discussion

Hypercholesterolaemia is well known as a major risk factor for
coronary atherosclerosis. There is interest in measuring blood cholesterol
levels in the young because there is increasing evidence that atherosclerosis
has its beginning in childhood [1, 2]. Tracking of high TC and TG levels from
childhood to adolescence and on into early adulthood is well documented in
Western populations [4-8]. The need for cholesterol determination on a
population basis and in the paediatric age group has been well described. One
strategy of population comparison is to select a specific age and sex group for
comparison across several populations. In our study, although most girls were
overweight, they represented a wide spectrum of body weights and lipid levels.
Our data revealed that the mean TC (194.27 mg/dl) and TG (160.07 mg/dl) serum
levels of normal adolescent Egyptian girls were high in comparison with levels
in other countries [21-26]. Unfortunately, no qualifying survey was found from
the Eastern Mediterranean region. The cause of these high levels requires
further investigation, but it may be related to nutritional habits, considering
the sedentary lifestyle of adolescent girls in Egypt. Gliksman et al. [27]
studied 5,211 schoolchildren aged 10 to 15 years and reported that BMI was the
highest, and aerobic fitness was the lowest, in children from Mediterranean and
Middle Eastern countries.

Because adolescence is a stage of pubertal development, we
decided to assess the Tanner stage when evaluating variables that might be
associated with adolescent growth. We found no association between Tanner stage
of puberty and lipid levels in this group of middle-school adolescent girls. Our
results confirm the findings of Omura et al. [28], who studied serum cholesterol
changes over a five-year period in 172 junior high school girls and found no
significant changes in serum cholesterol levels over this time. In other studies
[29, 30], no significant changes in lipids and lipoproteins were observed in
girls during sexual maturation changes or overall for the adolescent
period.

There is evidence that body composition in children and
adolescents may be more closely correlated with TC levels in certain ethnic
groups [31]. Lipidaemia and total cholesterolaemia increase with BMI [32]. In
women, BMI and waist circumference by themselves did as well as body-fat
distribution indices in explaining variation in TC and TG levels, suggesting the
involvement of visceral fat in the relation between disease and body fat or
body-fat distribution [33]. WHR has been used as an index of body-fat
distribution in several studies [34-36]. Other studies [18,19] used the ratios
arm circumference/thigh circumference and subscapular skinfold thickness/triceps
skinfold thickness to distinguish upper and central fat patterns.

Although our sample was small (n = 102), we found a
significant association between serum lipid levels and anthropometric indices of
body weight and fat distribution. The main factors affecting TC and TG levels in
our sample of adolescent girls seemed to be BMI and central body-fat pattern. In
fact, the variability of TC and TG levels explained by these two variables is
not as important as the fact that in their presence none of the measures of
anthropometry had any predictive value for TC and TG levels except abdominal
skinfold thickness for TG. The present results, as well as previous studies [9,
13], show that even in adolescents, a truncal distribution of adipose tissue is
related to elevated TC and TG serum levels.

TABLE 5. Results from the final model to predict the
variability of TC and TG a

Variables

TC partial r2(%)

TG partial r2 (%)

BMI

19.8

35.3

Central fat pattern

5.0

8.9

Abdominal skinfold thickness

3.3

total r2 =

24.8%

47.5%

F =

14.3

25.9

P =

0.0

0.0

a. Only girls having all study variables
were included in the analysis. The variables tested were BMI; suprailiac,
femoral, abdominal, and triceps/subscapular (central fat pattern) skinfold
thickness; and waist, thigh, and WHR circumferences.

WHR was not associated with TC level but was significantly
associated with TG level (p <.01). These results are in agreement with
other studies [11,13, 37] that found that WHR is associated with high
concentrations of TG and only weakly related to concentrations of TC. The
associations reported between WHR values and serum cholesterol concentrations in
adolescent children from the Healthy Examination Study of the United States [37]
may not reflect associations of TC with fat distribution, because changes in WHR
during adolescence are more likely to be reflections of changes in the pelvis
than in the adipose tissue. It is well demonstrated that during puberty and
adolescence boys deposit more fat in abdominal areas than do girls, whose fat is
predominantly localized on the hips [12]. These facts could explain the findings
that in girls, various measures of adiposity, such as BMI and skinfolds, are
related to lipid parameters, in contrast to boys, whose lipid levels are related
to WHR.

In conclusion, our findings demonstrate the high prevalence of
elevated levels of TC and TG in middle-class adolescent Egyptian girls and their
association with overweight and central fat pattern, thus providing the basis
for appropriate intervention by establishing school health education programmes
that include both vigorous physical activity and lipid screening. Preventing or
slowing the atherosclerotic process in childhood and adolescence could mean
years of healthy life for many people.

Rainer Gross and Werner Schultink are advisors of
the Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) at the
SEAMO-TROPMED Regional Center for Community Nutrition in Jakarta, Indonesia.
Imelda Angeles-Agdeppa is a doctoral student. Soemilah Sastroamidjojo and
Drupadi Dillon are staff members of the Center.

Abstract

Available information on iron deficiency and anaemia among
Indonesian population groups was analysed to identify the at-risk groups in
Indonesia and to suggest more efficient intervention programmes to reduce its
high prevalence. The results showed that the groups with the highest prevalence
of anaemia were pregnant women (52.3%), working adult women (27.9%),
pre-schoolers (27.1%), adolescent girls (21.1%), the elderly (10.9%), and
primary-school children (6.8%). Pre-school children and adolescents need iron
supplementation to provide enough iron for growth and cognitive functioning
during childhood. Adolescent girls need iron supplementation to develop
sufficient iron reserves before pregnancy and to improve working performance.
Pregnant and lactating women also need iron supplementation. Strategies to
control anaemia include improvement in dietary habits, food fortification, and
supplementation. Unless feeding behaviour is changed or food fortification is
adapted nationwide, oral iron supplementation remains the mainstay of the
prevention and treatment of anaemia. Weekly supplementation has been shown to be
an effective and economic method of supplementation. With the current approach
of daily supplementation recommended by the World Health Organization, Indonesia
would have to spend US$360 million annually, but weekly dosing would require
only US$15 million to cover the same target population. Weekly dosing offers a
practical and economic means of improving iron status in developing
countries.

Introduction

Anaemia is recognized as a major nutritional problem affecting
a majority of the women and children in developing countries. The World Health
Organization (WHO) estimates that more than two billion people are affected by
iron deficiency or anaemia. Most are in the Western Pacific and South-East Asia,
but they can be found in all countries [1]. Despite its increasing prevalence in
South-East Asia [2], anaemia is the most neglected nutritional deficiency
disorder in the region today [3]. The most affected groups, in approximate
descending order, are pregnant women, preschool-age children, low-birthweight
infants, other women of child-bearing age, the elderly, school-age children, and
adult men [1, 4].

Iron-deficiency anaemia has severe nutritional and health
consequences, including inadequate growth and mental development in children,
high maternal mortality, high incidence of low-birthweight infants, and low
productivity in adults [1]. Poor school performance among schoolchildren and
adolescents has been associated with iron-deficiency anaemia [5-7]. Low physical
performance was also observed in a group of adolescents in London [8].

In Indonesia, although some pilot studies on supplementation
trials among pre-school children have been conducted [9], routine oral iron
supplementation has been focused only on pregnant women [10]. Despite a national
programme for the last 20 years, the prevalence of anaemia decreased only slowly
from 70% in 1983 to between 55% and 60% in 1992 [11]. The main reasons for the
ineffectiveness of the programme are low compliance and inefficient delivery
systems [12, 13]. Another factor may be the late administration of supplements.
Pregnancy is the period of greatest demand for iron [14], but improving iron
nutrition during this period is difficult. The conventional target approach of
providing iron plus folate during the second trimester does not adequately
address the problem. Careful evaluation of the critical period when
supplementation should take place is required to minimize scarce budgetary
resources.

The present overview, based on the current experience gained
in Indonesia, describes population groups that are at high risk of anaemia and
analyses the effect of weekly dosing of iron so that future intervention
programmes can be initiated for not only curative but also preventive
purposes.

Prevalence of anaemia in different
population groups

Subjects were randomly chosen in each population group from a
series of cross-sectional surveys conducted in selected rural and urban areas in
Jakarta and Yogjakarta, Indonesia. The methods and results have been reported
[12, 13, 15-18]. Anaemia is defined here as haemoglobin levels <120 g/L among
adolescent girls and elderly women, <110 g/L among pre-school children and
pregnant women, and <130 g/L among adult and elderly men [19].

Figure 1 summarizes the prevalence of anaemia in different
Indonesian population groups. The average prevalence was highest among pregnant
women (52.3%). In both rural and urban areas, the prevalence of anaemia in
pregnant women was not associated with age (p >.05), but it was
associated with months of pregnancy (p <.001; X2
test) and whether they lived in a rural or an urban area. As shown in figure 2,
anaemia in rural areas appeared at a low rate in the third month of pregnancy
(18%) and was highest in the fifth month of pregnancy (75%). It decreased to 33%
at nine months. In urban areas, anaemia occurred as early as the second month of
pregnancy (50%) and reached a prevalence of 100% in the eighth month. Pregnant
women in this study belonged to the low- and middle-income groups; urban
pregnant women were more severely anaemic than rural ones (fig. 2). Suharno et
al. [20] found a similar prevalence of anaemia (49.4%) in pregnant women in West
Java. The most commonly identified reason for this high prevalence was the low
availability of iron in the rice-based Indonesian diet [21-23].

The prevalence of anaemia in non-pregnant women was 27.9%, and
no men were found to be anaemic. The prevalence of anaemia among adult women in
this study was lower than that among non-pregnant Chinese cotton mill workers
(34%) [24] but remained within the range of the prevalence of anaemia in
Indonesia nine years ago [11]. Iron supplements resulted in improved
productivity [9] and production efficiency [25]. Among the elderly, the
prevalence was higher in women (13.1%) than in men (8.9%).

The prevalence of anaemia among pre-school-age children was
26.4% for boys and 27.9% for girls, with a combined prevalence of 27.1%. The
prevalence of anaemia in pre-schoolers was not associated with sex (p
>.05; X2 test). The highest prevalence of anaemia (32% to
36%) was at 17 to 35 months of age in both boys and girls (fig. 3). The high
prevalence of anaemia (34.9%) in this study as early as 17 to 23 months reflects
depleted iron stores [26]. An even higher prevalence is found before 17 months
[27, 28]. During this period, the iron requirement is so high that breastmilk
alone cannot meet the requirement of iron for rapid growth [29]. Breastmilk
contains 0.5 mg iron per litre during the first month post-partum, falling to
about 0.3 mg/L at 4 to 6 months. Assuming a mean daily intake of 673 ml milk 1
month after birth and 896 ml at 6 months [30], the calculated daily iron intake
falls from 0.34 mg at 1 month to 0.27 mg at 6 months. Other factors, such as
repeated attacks of infectious diseases and the low content and bioavailability
of iron in the diet, put the young child at higher risk for anaemia. The
prevalence of anaemia decreased to 12.9% at 48 to 60 months (fig. 3). A lower
prevalence in this age group was also reported among Chinese [27] and Chilean
[28] pre-school children. This age-dependent dynamic of anaemia is consistent
with the epidemiology of nutritional anaemia [31]. The prevalence was 9.1% among
school-age boys but only 4.5% among school-age girls, with a combined prevalence
of 6.8%.

The prevalence was 21.1% in adolescent girls but only 2.5% in
adolescent boys. The high prevalence of anaemia among adolescent girls may be
due to menstrual losses, which average 38.0% ± 1.2% of the total iron
losses, and the occurrence of the second growth spurt [32] combined with low
dietary iron intake [33].

Current iron supplementation
programmes in Indonesia

The current programmes to control anaemia in Indonesia include
daily iron supplementation of pregnant women through the integrated health posts
and community health centres, nutrition education, and food fortification [10].
The low indication of improvement, as shown in this study, simply reflects the
limited effectiveness and sustainability of these programmes. To encourage
dietary modification, emphasis must be placed also on the diversity of food
produced and on improved access to these foods. Changing peoples behaviour
requires long and intensive national and community-based actions, such as mass
media campaigns and other formal and informal education in the community, that
support each other synergistically. Food fortification, the medium-term
strategy, offers benefits faster than dietary modification. However, many
operational problems may be encountered [1, 34].

The present high prevalence of anaemia in most age groups
justifies a broad intervention programme [35]. In developing countries, where
dietary iron is unlikely to be sufficient to overcome an iron deficit, iron
supplements are often relied upon as a cure for anaemia. This curative strategy
of giving iron supplements when the anaemia already exists is frequently of
limited effectiveness and sustainability because of poor compliance due to the
negative side-effects of daily dosing [13].

Weekly dosing in iron
supplementation

The Indonesian experience showed that the prevalence of
iron-deficiency anaemia is highest in preschool children and pregnant women.
These two peaks of prevalence have different causes: the high growth spurt in
infants, and menarche in women leading to depleted iron storage from blood loss.
The need for iron is aggravated during pregnancy. A curative approach alone is
not sufficiently effective to reduce markedly the high prevalence of anaemia in
pregnancy. Preventive iron supplementation of women before pregnancy is required
to prevent iron-deficiency anaemia during pregnancy. Dietary changes and food
fortification are important long-term strategies but cannot be expected to have
a rapid impact.

Several studies in different population groups have shown that
weekly dosing successfully reduces anaemia and is as effective as daily
administration in preschool children [15], adolescent girls [36], and
non-pregnant [37, 38] and pregnant [18] women.

Costs of iron
supplementation

WHO/UNICEF recommend that universal iron-folate
supplementation should be implemented for all pregnant and lactating women, for
infants and children six months through five years of age, and for
pre-adolescent girls and women from 10 to 49 years of age, in populations where
the prevalence of anaemia is over 30% [39]. In this recommendation, no specific
information is provided about when and for how long supplements should be
administered. However, an earlier recommendation [40] stated that in areas with
high prevalence, pregnant women should receive 60 mg elemental iron and 250
µg folate twice a day for 180 days, and normal infants should receive 1 mg
elemental iron per kilogram body weight per day from six months to five years of
age. Supplementation from the age of two months is recommended for
low-birthweight infants. For adolescent girls, 60 mg elemental iron twice a day
for two to three months is recommended. Table 1 shows the recommended duration
of iron supplementation for each intervention group. On the basis of a
calculation of the price of supplementation for the different intervention
groups, a yearly budget of US$360 million would be needed to follow the 1992 WHO
recommendation in Indonesia. Although the economic return would be higher
because of increased productivity and learning ability and fewer infections, it
would be unrealistic to expect an investment of this size for reducing
iron-deficiency anaemia alone.

TABLE 1. Duration of iron supplementation of different target
populations in Indonesia with the current WHO-recommended daily dosing approach
versus the suggested new weekly dosing approach

TABLE 2. Estimated annual cost of iron supplementation of
different target populations in Indonesia with the current WHO-recommended daily
dosing approach versus the suggested new weekly dosing approach

Target population

Millions of people(% of total) a

Cost in millions of US dollars

Current WHO approach

Suggested new approach

Pregnant and lactating women

5.5 (2.9)

3.9

0.5 b

Infants (0.5-1 yr)

1.9 (1.0)

11.4

1.6 c

Low-birthweight infants

0.5 (0.3) d

5.4

0.7 c

Pre-schoolers (>1 <5 yr)

19.7 (10.3)

315.2

10.5 c

Adolescent girls (10 -<19 yr)

29.9 (11.6)

23.6

1.6 b

Total

57.5 (25.8) e

359.5

14.9

a. Based on estimated 1996 population of
Indonesia (total, 191 million) Source: Directorate of Nutrition, Department of
Health, Indonesia.

On the basis of the experience gained in Indonesia, a
different approach is suggested for iron supplementation, which is shown in
table 2. This approach differs from the WHO approach mainly in two
aspects:

First, on the basis of the promising results in
Indonesia, weekly doses are suggested for all age groups. This will
reduce costs to one-seventh of the daily administration.

Second, it has been shown in pre-school children that iron
supplementation for eight weeks has an effect lasting for many months, until the
age when iron requirements decline and can be met by common food sources
[43].

When these two differences are taken into account, the yearly
budget for iron supplementation in Indonesia would be US$15 million, only 4.2%
of the cost of the strategy recommended by WHO.

Weekly supplementation not only is more efficient but also is
far less demanding of organizational and administrative efforts, because the
reduced number of tablets and syrup bottles allows an increase in the coverage
of the programme. In Indonesia traditional birth attendants have access to
pregnant and lactating mothers and low-birthweight infants. Schoolteachers have
contact with schoolchildren and adolescent girls, and factories employ many
non-pregnant women. All of these could be enlisted in support of weekly
supplementation. Weekly iron supplementation is cheaper and also offers
opportunities for wider coverage.

42. United Nations Administrative Committee on
Coordination/Subcommittee on Nutrition. Second report of the world nutrition
situation. Global and regional results. Geneva: United Nations Administrative
Committee on Coordination/Subcommittee on Nutrition, 1992.